diff --git a/packages/server/src/server/agent/agent-manager.test.ts b/packages/server/src/server/agent/agent-manager.test.ts
index 7635c58fc..c8d4e89c1 100644
--- a/packages/server/src/server/agent/agent-manager.test.ts
+++ b/packages/server/src/server/agent/agent-manager.test.ts
@@ -1,6 +1,6 @@
 import { expect, test, vi } from "vitest";
 import { spawn } from "node:child_process";
-import { mkdtempSync, rmSync } from "node:fs";
+import { mkdtempSync, rmSync, writeFileSync } from "node:fs";
 import { join } from "node:path";
 import { tmpdir } from "node:os";
 import { randomUUID } from "node:crypto";
@@ -8,6 +8,7 @@ import { randomUUID } from "node:crypto";
 import { createTestLogger } from "../../test-utils/test-logger.js";
 import {
   AgentManager,
+  AgentManagerShuttingDownError,
   commandMayHaveChangedExternalState,
   type AgentManagerEvent,
   type ManagedAgent,
@@ -139,6 +140,117 @@ class TestAgentClient implements AgentClient {
   }
 }
 
+class HeldAgentCreationClient extends TestAgentClient {
+  private readonly creationStarted = deferred<void>();
+  private readonly creationAllowed = deferred<void>();
+  createdSessionClosed = false;
+
+  override async createSession(config: AgentSessionConfig): Promise<AgentSession> {
+    const recordSessionClosed = () => {
+      this.createdSessionClosed = true;
+    };
+    const session = new (class extends TestAgentSession {
+      override async close(): Promise<void> {
+        recordSessionClosed();
+      }
+    })(config);
+    this.creationStarted.resolve();
+    await this.creationAllowed.promise;
+    return session;
+  }
+
+  waitForCreationToStart(): Promise<void> {
+    return this.creationStarted.promise;
+  }
+
+  finishCreating(): void {
+    this.creationAllowed.resolve();
+  }
+}
+
+class HeldAgentCreationAndCloseClient extends TestAgentClient {
+  private readonly creationStarted = deferred<void>();
+  private readonly creationAllowed = deferred<void>();
+  private readonly closeStarted = deferred<void>();
+  private readonly closeAllowed = deferred<void>();
+
+  override async createSession(config: AgentSessionConfig): Promise<AgentSession> {
+    this.creationStarted.resolve();
+    await this.creationAllowed.promise;
+    const signalCloseStarted = () => this.closeStarted.resolve();
+    const waitForClose = () => this.closeAllowed.promise;
+    return new (class extends TestAgentSession {
+      override async close(): Promise<void> {
+        signalCloseStarted();
+        await waitForClose();
+      }
+    })(config);
+  }
+
+  waitForCreationToStart(): Promise<void> {
+    return this.creationStarted.promise;
+  }
+
+  finishCreating(): void {
+    this.creationAllowed.resolve();
+  }
+
+  waitForCloseToStart(): Promise<void> {
+    return this.closeStarted.promise;
+  }
+
+  finishClosing(): void {
+    this.closeAllowed.resolve();
+  }
+}
+
+class HeldReloadCloseClient extends TestAgentClient {
+  private readonly closeStarted = deferred<void>();
+  private readonly closeAllowed = deferred<void>();
+  originalSessionClosed = false;
+  replacementSessionClosed = false;
+
+  override async createSession(config: AgentSessionConfig): Promise<AgentSession> {
+    const signalCloseStarted = () => this.closeStarted.resolve();
+    const waitForClose = () => this.closeAllowed.promise;
+    const recordOriginalClosed = () => {
+      this.originalSessionClosed = true;
+    };
+    return new (class extends TestAgentSession {
+      override async close(): Promise<void> {
+        signalCloseStarted();
+        await waitForClose();
+        recordOriginalClosed();
+      }
+    })(config);
+  }
+
+  override async resumeSession(
+    _handle: AgentPersistenceHandle,
+    config?: Partial<AgentSessionConfig>,
+  ): Promise<AgentSession> {
+    const recordReplacementClosed = () => {
+      this.replacementSessionClosed = true;
+    };
+    return new (class extends TestAgentSession {
+      override async close(): Promise<void> {
+        recordReplacementClosed();
+      }
+    })({
+      provider: "codex",
+      cwd: config?.cwd ?? process.cwd(),
+    });
+  }
+
+  waitForCloseToStart(): Promise<void> {
+    return this.closeStarted.promise;
+  }
+
+  finishClosing(): void {
+    this.closeAllowed.resolve();
+  }
+}
+
 class NativeArchiveRecordingClient extends TestAgentClient {
   readonly archivedHandles: AgentPersistenceHandle[] = [];
   readonly unarchivedHandles: AgentPersistenceHandle[] = [];
@@ -290,6 +402,52 @@ class TestAgentSession implements AgentSession {
   async close(): Promise<void> {}
 }
 
+class HeldRuntimeInfoSession extends TestAgentSession {
+  private readonly runtimeInfoRequested = deferred<void>();
+  private readonly runtimeInfoAllowed = deferred<void>();
+
+  override async getRuntimeInfo() {
+    this.runtimeInfoRequested.resolve();
+    await this.runtimeInfoAllowed.promise;
+    return await super.getRuntimeInfo();
+  }
+
+  waitForRuntimeInfo(): Promise<void> {
+    return this.runtimeInfoRequested.promise;
+  }
+
+  finishRuntimeInfo(): void {
+    this.runtimeInfoAllowed.resolve();
+  }
+}
+
+class HeldRuntimeInfoClient extends TestAgentClient {
+  private readonly sessionCreated = deferred<HeldRuntimeInfoSession>();
+  private session: HeldRuntimeInfoSession | null = null;
+
+  override async createSession(config: AgentSessionConfig): Promise<AgentSession> {
+    this.session = new HeldRuntimeInfoSession(config);
+    this.sessionCreated.resolve(this.session);
+    return this.session;
+  }
+
+  async waitForRuntimeInfo(): Promise<void> {
+    const session = await this.sessionCreated.promise;
+    await session.waitForRuntimeInfo();
+  }
+
+  finishRuntimeInfo(): void {
+    this.requireSession().finishRuntimeInfo();
+  }
+
+  private requireSession(): HeldRuntimeInfoSession {
+    if (!this.session) {
+      throw new Error("Expected a created session");
+    }
+    return this.session;
+  }
+}
+
 class StreamingAssistantSession implements AgentSession {
   readonly provider = "codex" as const;
   readonly capabilities = TEST_CAPABILITIES;
@@ -449,6 +607,211 @@ function fakeCodexEmitting(args: FakeCodexEmitterArgs): AgentClient {
 
 const logger = createTestLogger();
 
+test("does not register a session that finishes starting after shutdown begins", async () => {
+  const client = new HeldAgentCreationClient();
+  const manager = new AgentManager({
+    clients: { codex: client },
+    logger,
+    idFactory: () => "00000000-0000-4000-8000-000000000100",
+  });
+
+  const creation = manager.createAgent(
+    {
+      provider: "codex",
+      cwd: process.cwd(),
+    },
+    undefined,
+    { workspaceId: undefined },
+  );
+  await client.waitForCreationToStart();
+
+  manager.prepareForShutdown();
+  client.finishCreating();
+
+  await expect(creation).rejects.toThrow("Agent manager is shutting down");
+  expect({ agents: manager.listAgents(), sessionClosed: client.createdSessionClosed }).toEqual({
+    agents: [],
+    sessionClosed: true,
+  });
+});
+
+test("flush waits for rejected session cleanup that starts after shutdown", async () => {
+  const client = new HeldAgentCreationAndCloseClient();
+  const manager = new AgentManager({
+    clients: { codex: client },
+    logger,
+    idFactory: () => "00000000-0000-4000-8000-000000000098",
+  });
+
+  const creation = manager
+    .createAgent(
+      {
+        provider: "codex",
+        cwd: process.cwd(),
+      },
+      undefined,
+      { workspaceId: undefined },
+    )
+    .catch((error: unknown) => error);
+  await client.waitForCreationToStart();
+
+  manager.prepareForShutdown();
+  let flushResolved = false;
+  const flushing = manager.flushForShutdown().then(() => {
+    flushResolved = true;
+    return undefined;
+  });
+  client.finishCreating();
+  await client.waitForCloseToStart();
+
+  try {
+    expect(flushResolved).toBe(false);
+  } finally {
+    client.finishClosing();
+  }
+
+  expect(await creation).toBeInstanceOf(AgentManagerShuttingDownError);
+  await flushing;
+  expect(manager.listAgents()).toEqual([]);
+});
+
+test("does not persist an initializing session after shutdown closes it", async () => {
+  const workdir = mkdtempSync(join(tmpdir(), "agent-manager-shutdown-register-test-"));
+  const storage = new AgentStorage(join(workdir, "agents"), logger);
+  const client = new HeldRuntimeInfoClient();
+  const agentId = "00000000-0000-4000-8000-000000000099";
+  const manager = new AgentManager({
+    clients: { codex: client },
+    registry: storage,
+    logger,
+    idFactory: () => agentId,
+  });
+
+  try {
+    const creation = manager.createAgent(
+      {
+        provider: "codex",
+        cwd: workdir,
+      },
+      undefined,
+      { workspaceId: undefined },
+    );
+    await client.waitForRuntimeInfo();
+
+    manager.prepareForShutdown();
+    const closing = manager.closeAgent(agentId);
+    client.finishRuntimeInfo();
+
+    await expect(creation).rejects.toBeInstanceOf(AgentManagerShuttingDownError);
+    await closing;
+    await storage.flush();
+    expect({ agents: manager.listAgents(), record: await storage.get(agentId) }).toMatchObject({
+      agents: [],
+      record: { lastStatus: "closed" },
+    });
+  } finally {
+    rmSync(workdir, { recursive: true, force: true });
+  }
+});
+
+test("reload leaves a closed durable snapshot when shutdown starts during the swap", async () => {
+  const workdir = mkdtempSync(join(tmpdir(), "agent-manager-shutdown-reload-test-"));
+  const storage = new AgentStorage(join(workdir, "agents"), logger);
+  const client = new HeldReloadCloseClient();
+  const agentId = "00000000-0000-4000-8000-000000000097";
+  const manager = new AgentManager({
+    clients: { codex: client },
+    registry: storage,
+    logger,
+    idFactory: () => agentId,
+  });
+
+  try {
+    await manager.createAgent(
+      {
+        provider: "codex",
+        cwd: workdir,
+      },
+      undefined,
+      { workspaceId: undefined },
+    );
+    const reload = manager.reloadAgentSession(agentId).catch((error: unknown) => error);
+    await client.waitForCloseToStart();
+
+    manager.prepareForShutdown();
+    const closing = Promise.all(manager.listAgents().map((agent) => manager.closeAgent(agent.id)));
+    client.finishClosing();
+
+    await closing;
+    expect(await reload).toBeInstanceOf(AgentManagerShuttingDownError);
+    await manager.flush();
+    await storage.flush();
+    expect({
+      agents: manager.listAgents(),
+      record: await storage.get(agentId),
+      replacementSessionClosed: client.replacementSessionClosed,
+    }).toMatchObject({
+      agents: [],
+      record: { lastStatus: "closed" },
+      replacementSessionClosed: true,
+    });
+  } finally {
+    client.finishClosing();
+    await manager.flush().catch(() => undefined);
+    await storage.flush().catch(() => undefined);
+    rmSync(workdir, { recursive: true, force: true });
+  }
+});
+
+test("reload closes both sessions when the closed snapshot cannot be persisted", async () => {
+  const workdir = mkdtempSync(join(tmpdir(), "agent-manager-reload-persist-failure-test-"));
+  const storagePath = join(workdir, "agents");
+  const storage = new AgentStorage(storagePath, logger);
+  const client = new HeldReloadCloseClient();
+  const agentId = "00000000-0000-4000-8000-000000000096";
+  const manager = new AgentManager({
+    clients: { codex: client },
+    registry: storage,
+    logger,
+    idFactory: () => agentId,
+  });
+
+  try {
+    await manager.createAgent(
+      {
+        provider: "codex",
+        cwd: workdir,
+      },
+      undefined,
+      { workspaceId: undefined },
+    );
+    await storage.flush();
+    rmSync(storagePath, { recursive: true, force: true });
+    writeFileSync(storagePath, "blocks the storage directory");
+
+    const reload = manager.reloadAgentSession(agentId).catch((error: unknown) => error);
+    await client.waitForCloseToStart();
+    client.finishClosing();
+
+    expect(await reload).toBeInstanceOf(Error);
+    await manager.flushForShutdown();
+    expect({
+      agents: manager.listAgents(),
+      originalSessionClosed: client.originalSessionClosed,
+      replacementSessionClosed: client.replacementSessionClosed,
+    }).toEqual({
+      agents: [],
+      originalSessionClosed: true,
+      replacementSessionClosed: true,
+    });
+  } finally {
+    client.finishClosing();
+    await manager.flushForShutdown().catch(() => undefined);
+    await storage.flush().catch(() => undefined);
+    rmSync(workdir, { recursive: true, force: true });
+  }
+});
+
 test("normalizeConfig injects the provider default model when omitted", async () => {
   const workdir = mkdtempSync(join(tmpdir(), "agent-manager-test-"));
   const storagePath = join(workdir, "agents");
diff --git a/packages/server/src/server/agent/agent-manager.ts b/packages/server/src/server/agent/agent-manager.ts
index 48ad8bcf7..232f5c57a 100644
--- a/packages/server/src/server/agent/agent-manager.ts
+++ b/packages/server/src/server/agent/agent-manager.ts
@@ -82,6 +82,13 @@ const STORED_AGENT_CAPABILITIES: AgentCapabilityFlags = {
 
 type TimeoutResult = "completed" | "timed_out";
 
+export class AgentManagerShuttingDownError extends Error {
+  constructor() {
+    super("Agent manager is shutting down");
+    this.name = "AgentManagerShuttingDownError";
+  }
+}
+
 interface PreparedSessionConfig {
   storedConfig: AgentSessionConfig;
   launchConfig: AgentSessionConfig;
@@ -535,6 +542,7 @@ export class AgentManager {
   private readonly durableTimelineStore?: AgentTimelineStore;
   private readonly previousStatuses = new Map<string, AgentLifecycleStatus>();
   private readonly backgroundTasks = new Set<Promise<void>>();
+  private readonly agentRegistrationTasks = new Set<Promise<void>>();
   private readonly agentStreamCoalescer: AgentStreamCoalescer;
   private mcpBaseUrl: string | null;
   private readonly mcpAuthToken: string | null;
@@ -546,6 +554,7 @@ export class AgentManager {
   private onWorkspaceStateMayHaveChanged?: (params: { cwd: string }) => void;
   private logger: Logger;
   private readonly rescueTimeouts: Required<AgentManagerRescueTimeouts>;
+  private acceptingAgentRegistrations = true;
 
   constructor(options: AgentManagerOptions) {
     this.idFactory = options?.idFactory ?? (() => randomUUID());
@@ -619,6 +628,10 @@ export class AgentManager {
     this.mcpBaseUrl = url;
   }
 
+  prepareForShutdown(): void {
+    this.acceptingAgentRegistrations = false;
+  }
+
   setPaseoToolsEnabled(enabled: boolean): void {
     this.paseoToolsEnabled = enabled;
   }
@@ -922,11 +935,20 @@ export class AgentManager {
     return this.timelineStore.fetch(id, options);
   }
 
-  async createAgent(
+  createAgent(
     config: AgentSessionConfig,
     agentId: string | undefined,
     options: CreateAgentOptions,
   ): Promise<ManagedAgent> {
+    return this.trackAgentRegistrationOperation(this.createAgentInternal(config, agentId, options));
+  }
+
+  private async createAgentInternal(
+    config: AgentSessionConfig,
+    agentId: string | undefined,
+    options: CreateAgentOptions,
+  ): Promise<ManagedAgent> {
+    this.assertAcceptingAgentRegistrations();
     const resolvedAgentId = validateAgentId(agentId ?? this.idFactory(), "createAgent");
     const { storedConfig, launchConfig } = await this.prepareSessionConfig(config, resolvedAgentId);
     this.requireEnabledProvider(storedConfig.provider);
@@ -954,7 +976,7 @@ export class AgentManager {
 
   // Reconstruct an agent from provider persistence. Callers should explicitly
   // hydrate timeline history after resume.
-  async resumeAgentFromPersistence(
+  resumeAgentFromPersistence(
     handle: AgentPersistenceHandle,
     overrides?: Partial<AgentSessionConfig>,
     agentId?: string,
@@ -966,6 +988,24 @@ export class AgentManager {
       workspaceId?: string;
     },
   ): Promise<ManagedAgent> {
+    return this.trackAgentRegistrationOperation(
+      this.resumeAgentFromPersistenceInternal(handle, overrides, agentId, options),
+    );
+  }
+
+  private async resumeAgentFromPersistenceInternal(
+    handle: AgentPersistenceHandle,
+    overrides?: Partial<AgentSessionConfig>,
+    agentId?: string,
+    options?: {
+      createdAt?: Date;
+      updatedAt?: Date;
+      lastUserMessageAt?: Date | null;
+      labels?: Record<string, string>;
+      workspaceId?: string;
+    },
+  ): Promise<ManagedAgent> {
+    this.assertAcceptingAgentRegistrations();
     const resolvedAgentId = validateAgentId(
       agentId ?? this.idFactory(),
       "resumeAgentFromPersistence",
@@ -994,13 +1034,24 @@ export class AgentManager {
     return this.registerSession(session, storedConfig, resolvedAgentId, options);
   }
 
-  async importProviderSession(input: {
+  importProviderSession(input: {
     provider: AgentProvider;
     providerHandleId: string;
     cwd: string;
     workspaceId: string;
     labels?: Record<string, string>;
   }): Promise<ManagedAgent> {
+    return this.trackAgentRegistrationOperation(this.importProviderSessionInternal(input));
+  }
+
+  private async importProviderSessionInternal(input: {
+    provider: AgentProvider;
+    providerHandleId: string;
+    cwd: string;
+    workspaceId: string;
+    labels?: Record<string, string>;
+  }): Promise<ManagedAgent> {
+    this.assertAcceptingAgentRegistrations();
     const resolvedAgentId = validateAgentId(this.idFactory(), "importProviderSession");
     this.requireEnabledProvider(input.provider);
 
@@ -1025,20 +1076,30 @@ export class AgentManager {
       },
       { config: providerLaunchConfig, storedConfig, launchContext },
     );
-    const importedConfig = await this.normalizeConfig(stripInternalPaseoMcpServer(imported.config));
-    const timelineRows = buildImportedTimelineRows(imported.timeline);
-    const initialTitle = resolveImportedAgentTitle(importedConfig, timelineRows);
+    let handedToRegistration = false;
+    try {
+      const importedConfig = await this.normalizeConfig(
+        stripInternalPaseoMcpServer(imported.config),
+      );
+      const timelineRows = buildImportedTimelineRows(imported.timeline);
+      const initialTitle = resolveImportedAgentTitle(importedConfig, timelineRows);
 
-    return this.registerSession(imported.session, importedConfig, resolvedAgentId, {
-      labels: input.labels,
-      workspaceId: input.workspaceId,
-      timelineRows,
-      timelineNextSeq: timelineRows.length + 1,
-      persistence: imported.persistence,
-      historyPrimed: true,
-      initialTitle,
-      publishWhenReady: true,
-    });
+      handedToRegistration = true;
+      return this.registerSession(imported.session, importedConfig, resolvedAgentId, {
+        labels: input.labels,
+        workspaceId: input.workspaceId,
+        timelineRows,
+        timelineNextSeq: timelineRows.length + 1,
+        persistence: imported.persistence,
+        historyPrimed: true,
+        initialTitle,
+        publishWhenReady: true,
+      });
+    } finally {
+      if (!handedToRegistration) {
+        await this.closeUnregisteredSession(imported.session);
+      }
+    }
   }
 
   // Hot-reload an active agent session with config overrides. By default the
@@ -1047,11 +1108,22 @@ export class AgentManager {
   // new epoch is minted and provider history is re-streamed — this is what the
   // user-facing "Reload agent" action wants when the on-disk session was
   // mutated outside Paseo.
-  async reloadAgentSession(
+  reloadAgentSession(
     agentId: string,
     overrides?: Partial<AgentSessionConfig>,
     options?: { rehydrateFromDisk?: boolean },
   ): Promise<ManagedAgent> {
+    return this.trackAgentRegistrationOperation(
+      this.reloadAgentSessionInternal(agentId, overrides, options),
+    );
+  }
+
+  private async reloadAgentSessionInternal(
+    agentId: string,
+    overrides?: Partial<AgentSessionConfig>,
+    options?: { rehydrateFromDisk?: boolean },
+  ): Promise<ManagedAgent> {
+    this.assertAcceptingAgentRegistrations();
     let existing = this.requireSessionAgent(agentId);
     if (this.hasInFlightRun(agentId)) {
       await this.cancelAgentRun(agentId);
@@ -1078,36 +1150,43 @@ export class AgentManager {
       ? await client.resumeSession(handle, providerLaunchConfig, launchContext)
       : await client.createSession(providerLaunchConfig, launchContext);
 
-    this.agentStreamCoalescer.flushAndDiscard(agentId);
-    // Remove the existing agent entry before swapping sessions
-    this.agents.delete(agentId);
-    if (existing.unsubscribeSession) {
-      existing.unsubscribeSession();
-      existing.unsubscribeSession = null;
-    }
-    this.foregroundRuns.clearAgent(agentId, existing);
-    await this.closeReloadedSession(existing.session, agentId);
+    let handedToRegistration = false;
+    try {
+      this.assertAcceptingAgentRegistrations();
 
-    if (rehydrateFromDisk) {
-      // Wipe both durable and in-memory timeline so registerSession mints a
-      // new epoch and hydrateTimelineFromProvider re-streams the freshly read
-      // provider history into an empty timeline.
-      await this.deleteCommittedTimeline(agentId);
-      this.timelineStore.delete(agentId);
-    }
+      const closedExisting = this.prepareAgentForClosure(existing, "agent reloaded");
+      try {
+        await this.persistSnapshot(closedExisting);
+      } finally {
+        await this.closeReloadedSession(existing.session, agentId);
+      }
 
-    // Preserve existing labels and timeline during reload.
-    return this.registerSession(session, storedConfig, agentId, {
-      labels: existing.labels,
-      workspaceId: existing.workspaceId,
-      createdAt: existing.createdAt,
-      updatedAt: existing.updatedAt,
-      lastUserMessageAt: existing.lastUserMessageAt,
-      historyPrimed: rehydrateFromDisk ? false : preservedHistoryPrimed,
-      lastUsage: preservedLastUsage,
-      lastError: preservedLastError,
-      attention: preservedAttention,
-    });
+      if (rehydrateFromDisk) {
+        // Wipe both durable and in-memory timeline so registerSession mints a
+        // new epoch and hydrateTimelineFromProvider re-streams the freshly read
+        // provider history into an empty timeline.
+        await this.deleteCommittedTimeline(agentId);
+        this.timelineStore.delete(agentId);
+      }
+
+      // Preserve existing labels and timeline during reload.
+      handedToRegistration = true;
+      return this.registerSession(session, storedConfig, agentId, {
+        labels: existing.labels,
+        workspaceId: existing.workspaceId,
+        createdAt: existing.createdAt,
+        updatedAt: existing.updatedAt,
+        lastUserMessageAt: existing.lastUserMessageAt,
+        historyPrimed: rehydrateFromDisk ? false : preservedHistoryPrimed,
+        lastUsage: preservedLastUsage,
+        lastError: preservedLastError,
+        attention: preservedAttention,
+      });
+    } finally {
+      if (!handedToRegistration) {
+        await this.closeUnregisteredSession(session);
+      }
+    }
   }
 
   private async closeReloadedSession(session: AgentSession, agentId: string): Promise<void> {
@@ -2474,49 +2553,84 @@ export class AgentManager {
       workspaceId?: string;
     },
   ): Promise<ManagedAgent> {
-    const resolvedAgentId = validateAgentId(agentId, "registerSession");
-    if (this.agents.has(resolvedAgentId)) {
-      throw new Error(`Agent with id ${resolvedAgentId} already exists`);
-    }
-    const initialPersistedTitle = await this.resolveInitialPersistedTitle(
-      resolvedAgentId,
-      config,
-      options?.initialTitle ?? null,
-    );
+    let registered = false;
+    try {
+      this.assertAcceptingAgentRegistrations();
+      const resolvedAgentId = validateAgentId(agentId, "registerSession");
+      if (this.agents.has(resolvedAgentId)) {
+        throw new Error(`Agent with id ${resolvedAgentId} already exists`);
+      }
+      const initialPersistedTitle = await this.resolveInitialPersistedTitle(
+        resolvedAgentId,
+        config,
+        options?.initialTitle ?? null,
+      );
 
-    const now = new Date();
-    const { durableTimelineHasRows } = await this.initializeAgentTimelineForRegister({
-      agentId: resolvedAgentId,
-      now,
-      options,
-    });
+      const now = new Date();
+      const { durableTimelineHasRows } = await this.initializeAgentTimelineForRegister({
+        agentId: resolvedAgentId,
+        now,
+        options,
+      });
 
-    const managed = this.buildManagedAgentForRegister({
-      resolvedAgentId,
-      session,
-      config,
-      now,
-      durableTimelineHasRows,
-      options,
-    });
+      const managed = this.buildManagedAgentForRegister({
+        resolvedAgentId,
+        session,
+        config,
+        now,
+        durableTimelineHasRows,
+        options,
+      });
 
-    this.agents.set(resolvedAgentId, managed);
-    // Initialize previousStatus to track transitions
-    this.previousStatuses.set(resolvedAgentId, managed.lifecycle);
-    await this.refreshRuntimeInfo(managed, { emit: !options?.publishWhenReady });
-    await this.persistSnapshot(managed, {
-      title: initialPersistedTitle,
-    });
-    if (!options?.publishWhenReady) {
+      this.assertAcceptingAgentRegistrations();
+      this.agents.set(resolvedAgentId, managed);
+      registered = true;
+      // Initialize previousStatus to track transitions
+      this.previousStatuses.set(resolvedAgentId, managed.lifecycle);
+      await this.refreshRuntimeInfo(managed, { emit: false });
+      this.assertAgentRegistrationActive(managed);
+      await this.persistSnapshot(managed, {
+        title: initialPersistedTitle,
+      });
+      this.assertAgentRegistrationActive(managed);
+      if (!options?.publishWhenReady) {
+        this.emitState(managed, { persist: false });
+      }
+
+      await this.refreshSessionState(managed, { emit: false });
+      this.assertAgentRegistrationActive(managed);
+      managed.lifecycle = "idle";
+      await this.persistSnapshot(managed);
+      this.assertAgentRegistrationActive(managed);
       this.emitState(managed, { persist: false });
+      this.subscribeToSession(managed);
+      return { ...managed };
+    } catch (error) {
+      if (!registered) {
+        await this.closeUnregisteredSession(session);
+      }
+      throw error;
     }
+  }
 
-    await this.refreshSessionState(managed, { emit: !options?.publishWhenReady });
-    managed.lifecycle = "idle";
-    await this.persistSnapshot(managed);
-    this.emitState(managed, { persist: false });
-    this.subscribeToSession(managed);
-    return { ...managed };
+  private assertAcceptingAgentRegistrations(): void {
+    if (!this.acceptingAgentRegistrations) {
+      throw new AgentManagerShuttingDownError();
+    }
+  }
+
+  private assertAgentRegistrationActive(agent: ActiveManagedAgent): void {
+    if (!this.acceptingAgentRegistrations || this.agents.get(agent.id) !== agent) {
+      throw new AgentManagerShuttingDownError();
+    }
+  }
+
+  private async closeUnregisteredSession(session: AgentSession): Promise<void> {
+    try {
+      await session.close();
+    } catch (error) {
+      this.logger.warn({ err: error }, "Failed to close unregistered agent session");
+    }
   }
 
   private async initializeAgentTimelineForRegister(params: {
@@ -3565,15 +3679,45 @@ export class AgentManager {
     });
   }
 
+  private trackAgentRegistrationOperation<T>(result: Promise<T>): Promise<T> {
+    const settled = result.then(
+      () => undefined,
+      () => undefined,
+    );
+    this.agentRegistrationTasks.add(settled);
+    void settled.then(() => {
+      this.agentRegistrationTasks.delete(settled);
+      return undefined;
+    });
+    return result;
+  }
+
   /**
    * Flush any background persistence work (best-effort).
-   * Used by daemon shutdown paths to avoid unhandled rejections after cleanup.
    */
   async flush(): Promise<void> {
+    await this.flushTasks({ includeAgentRegistrations: false });
+  }
+
+  /**
+   * Flush persistence and agent registrations that crossed the synchronous
+   * shutdown barrier. Those registrations own provider sessions until they
+   * either install them or close them.
+   */
+  async flushForShutdown(): Promise<void> {
+    await this.flushTasks({ includeAgentRegistrations: true });
+  }
+
+  private async flushTasks(options: { includeAgentRegistrations: boolean }): Promise<void> {
     this.agentStreamCoalescer.flushAll();
     // Drain tasks, including tasks spawned while awaiting.
-    while (this.backgroundTasks.size > 0) {
-      const pending = Array.from(this.backgroundTasks);
+    while (
+      this.backgroundTasks.size > 0 ||
+      (options.includeAgentRegistrations && this.agentRegistrationTasks.size > 0)
+    ) {
+      const pending = options.includeAgentRegistrations
+        ? [...this.backgroundTasks, ...this.agentRegistrationTasks]
+        : [...this.backgroundTasks];
       await Promise.allSettled(pending);
     }
   }
diff --git a/packages/server/src/server/bootstrap.smoke.test.ts b/packages/server/src/server/bootstrap.smoke.test.ts
index d4e6bbff5..5f762fa24 100644
--- a/packages/server/src/server/bootstrap.smoke.test.ts
+++ b/packages/server/src/server/bootstrap.smoke.test.ts
@@ -7,6 +7,7 @@ import { afterEach, describe, expect, test, vi } from "vitest";
 import { WebSocket } from "ws";
 
 import { createPaseoDaemon, parseListenString, type PaseoDaemonConfig } from "./bootstrap.js";
+import { AgentManagerShuttingDownError } from "./agent/agent-manager.js";
 import { hashDaemonPassword } from "./auth.js";
 import { generateLocalPairingOffer } from "./pairing-offer.js";
 import { createTestPaseoDaemon } from "./test-utils/paseo-daemon.js";
@@ -14,6 +15,23 @@ import { createTestAgentClients } from "./test-utils/fake-agent-client.js";
 import { isPlatform } from "../test-utils/platform.js";
 import { findFreePort } from "./service-proxy.js";
 
+interface HeldAgentClose {
+  started: Promise<void>;
+  arm(): void;
+  closeSession(): Promise<void>;
+  finish(): void;
+}
+
+interface BlockedDaemonShutdown {
+  probeReconnect(): Promise<WebSocketProbeResult>;
+  tryCreateAgent(): Promise<"created" | "rejected">;
+  finish(): Promise<void>;
+}
+
+type WebSocketProbeResult =
+  | { status: "connected" }
+  | { status: "rejected"; statusCode: number | null };
+
 describe("paseo daemon bootstrap", () => {
   afterEach(() => {
     vi.restoreAllMocks();
@@ -206,6 +224,17 @@ describe("paseo daemon bootstrap", () => {
     }
   });
 
+  test("stops new connections and agent registrations before closing agents", async () => {
+    const shutdown = await beginDaemonShutdownWithAgentClosing();
+    try {
+      await expect(
+        Promise.all([shutdown.probeReconnect(), shutdown.tryCreateAgent()]),
+      ).resolves.toEqual([{ status: "rejected", statusCode: 503 }, "rejected"]);
+    } finally {
+      await shutdown.finish();
+    }
+  });
+
   test("standalone listener exposes services only", async () => {
     const standalonePort = await findFreePort();
     const upstream = http.createServer((_req, res) => {
@@ -522,3 +551,97 @@ describe("paseo daemon bootstrap", () => {
     },
   );
 });
+
+function holdAgentClose(): HeldAgentClose {
+  let armed = false;
+  let markStarted = () => {};
+  let finish = () => {};
+  const started = new Promise<void>((resolve) => {
+    markStarted = resolve;
+  });
+  const finished = new Promise<void>((resolve) => {
+    finish = resolve;
+  });
+  return {
+    started,
+    arm() {
+      armed = true;
+    },
+    async closeSession() {
+      if (!armed) {
+        return;
+      }
+      markStarted();
+      await finished;
+    },
+    finish: () => finish(),
+  };
+}
+
+async function beginDaemonShutdownWithAgentClosing(): Promise<BlockedDaemonShutdown> {
+  const heldAgentClose = holdAgentClose();
+  const daemonHandle = await createTestPaseoDaemon({
+    cleanup: false,
+    agentClients: createTestAgentClients({ closeSession: heldAgentClose.closeSession }),
+  });
+  const agentCwd = await mkdtemp(path.join(os.tmpdir(), "paseo-shutdown-agent-"));
+  await daemonHandle.daemon.agentManager.createAgent(
+    {
+      provider: "codex",
+      cwd: agentCwd,
+    },
+    undefined,
+    { workspaceId: undefined },
+  );
+
+  heldAgentClose.arm();
+  const stopPromise = daemonHandle.daemon.stop();
+  await heldAgentClose.started;
+
+  return {
+    probeReconnect: () => probeWebSocketConnection(`ws://127.0.0.1:${daemonHandle.port}/ws`),
+    async tryCreateAgent() {
+      try {
+        await daemonHandle.daemon.agentManager.createAgent(
+          {
+            provider: "codex",
+            cwd: agentCwd,
+          },
+          undefined,
+          { workspaceId: undefined },
+        );
+        return "created";
+      } catch (error) {
+        if (error instanceof AgentManagerShuttingDownError) {
+          return "rejected";
+        }
+        throw error;
+      }
+    },
+    async finish() {
+      heldAgentClose.finish();
+      await stopPromise;
+      await daemonHandle.daemon.agentManager.flush().catch(() => undefined);
+      await Promise.all([
+        rm(path.dirname(daemonHandle.paseoHome), { recursive: true, force: true }),
+        rm(daemonHandle.staticDir, { recursive: true, force: true }),
+        rm(agentCwd, { recursive: true, force: true }),
+      ]);
+    },
+  };
+}
+
+function probeWebSocketConnection(url: string): Promise<WebSocketProbeResult> {
+  const ws = new WebSocket(url);
+  return new Promise((resolve) => {
+    ws.once("open", () => {
+      ws.close();
+      resolve({ status: "connected" });
+    });
+    ws.once("error", () => resolve({ status: "rejected", statusCode: null }));
+    ws.once("unexpected-response", (_request, response) => {
+      response.resume();
+      resolve({ status: "rejected", statusCode: response.statusCode ?? null });
+    });
+  });
+}
diff --git a/packages/server/src/server/bootstrap.ts b/packages/server/src/server/bootstrap.ts
index 0d86b08f7..2c0b2885f 100644
--- a/packages/server/src/server/bootstrap.ts
+++ b/packages/server/src/server/bootstrap.ts
@@ -1443,8 +1443,11 @@ export async function createPaseoDaemon(
 
   const stop = async () => {
     scriptHealthMonitor.stop();
+    // Freeze both ingress and registration before taking the agent closure snapshot.
+    wsServer?.prepareForShutdown();
+    agentManager.prepareForShutdown();
     await closeAllAgents(logger, agentManager);
-    await agentManager.flush().catch(() => undefined);
+    await agentManager.flushForShutdown().catch(() => undefined);
     detachAgentStoragePersistence();
     await agentStorage.flush().catch(() => undefined);
     await providerSnapshotManager.shutdown();
diff --git a/packages/server/src/server/test-utils/fake-agent-client.ts b/packages/server/src/server/test-utils/fake-agent-client.ts
index 81335f6f8..6468f9fb1 100644
--- a/packages/server/src/server/test-utils/fake-agent-client.ts
+++ b/packages/server/src/server/test-utils/fake-agent-client.ts
@@ -51,6 +51,18 @@ interface Deferred<T> {
   reject: (err: unknown) => void;
 }
 
+interface FakeAgentSessionOptions {
+  providerName: string;
+  config: AgentSessionConfig;
+  sessionId?: string;
+  memoryMarker?: string | null;
+  closeSession?: () => Promise<void>;
+}
+
+export interface TestAgentClientOptions {
+  closeSession?: () => Promise<void>;
+}
+
 function createDeferred<T>(): Deferred<T> {
   let resolve!: (value: T) => void;
   let reject!: (err: unknown) => void;
@@ -316,16 +328,14 @@ class FakeAgentSession implements AgentSession {
   private nextTurnOrdinal = 0;
   private activeForegroundTurnId: string | null = null;
 
-  constructor(
-    providerName: string,
-    config: AgentSessionConfig,
-    sessionId?: string,
-    memoryMarker?: string | null,
-  ) {
-    this.providerName = providerName;
-    this.config = config;
-    this.id = sessionId ?? randomUUID();
-    this.memoryMarker = memoryMarker ?? null;
+  private readonly closeSession: (() => Promise<void>) | undefined;
+
+  constructor(options: FakeAgentSessionOptions) {
+    this.providerName = options.providerName;
+    this.config = options.config;
+    this.id = options.sessionId ?? randomUUID();
+    this.memoryMarker = options.memoryMarker ?? null;
+    this.closeSession = options.closeSession;
     this.historyPath = path.join(
       tmpdir(),
       "paseo-fake-provider-history",
@@ -847,7 +857,9 @@ class FakeAgentSession implements AgentSession {
     this.interruptSignal.resolve();
   }
 
-  async close(): Promise<void> {}
+  async close(): Promise<void> {
+    await this.closeSession?.();
+  }
 
   async listCommands(): Promise<AgentSlashCommand[]> {
     if (this.providerName === "codex") {
@@ -1155,13 +1167,20 @@ class FakeAgentSession implements AgentSession {
 
 class FakeAgentClient implements AgentClient {
   readonly capabilities = TEST_CAPABILITIES;
-  constructor(public readonly provider: string) {}
+  constructor(
+    public readonly provider: string,
+    private readonly options: TestAgentClientOptions,
+  ) {}
 
   async createSession(
     config: AgentSessionConfig,
     _launchContext?: AgentLaunchContext,
   ): Promise<AgentSession> {
-    return new FakeAgentSession(this.provider, { ...config });
+    return new FakeAgentSession({
+      providerName: this.provider,
+      config: { ...config },
+      closeSession: this.options.closeSession,
+    });
   }
 
   async resumeSession(
@@ -1178,12 +1197,13 @@ class FakeAgentClient implements AgentClient {
       (handle.metadata as Record<string, unknown> | undefined)?.marker ??
       (handle.metadata as Record<string, unknown> | undefined)?.conversationId ??
       null;
-    return new FakeAgentSession(
-      this.provider,
-      cfg,
-      handle.sessionId,
-      typeof marker === "string" ? marker : null,
-    );
+    return new FakeAgentSession({
+      providerName: this.provider,
+      config: cfg,
+      sessionId: handle.sessionId,
+      memoryMarker: typeof marker === "string" ? marker : null,
+      closeSession: this.options.closeSession,
+    });
   }
 
   async fetchCatalog(
@@ -1222,10 +1242,12 @@ class FakeAgentClient implements AgentClient {
   }
 }
 
-export function createTestAgentClients(): Record<string, AgentClient> {
+export function createTestAgentClients(
+  options: TestAgentClientOptions = {},
+): Record<string, AgentClient> {
   return {
-    claude: new FakeAgentClient("claude"),
-    codex: new FakeAgentClient("codex"),
-    opencode: new FakeAgentClient("opencode"),
+    claude: new FakeAgentClient("claude", options),
+    codex: new FakeAgentClient("codex", options),
+    opencode: new FakeAgentClient("opencode", options),
   };
 }
diff --git a/packages/server/src/server/websocket-server.relay-reconnect.test.ts b/packages/server/src/server/websocket-server.relay-reconnect.test.ts
index 64e2918fe..be49b8dae 100644
--- a/packages/server/src/server/websocket-server.relay-reconnect.test.ts
+++ b/packages/server/src/server/websocket-server.relay-reconnect.test.ts
@@ -454,6 +454,21 @@ function holdNextSessionMessage(session: (typeof sessionMock.instances)[number])
   };
 }
 
+function holdSessionCleanup(session: (typeof sessionMock.instances)[number]): {
+  finish: () => void;
+} {
+  let finish = () => {};
+  session.cleanup.mockImplementationOnce(
+    () =>
+      new Promise<void>((resolve) => {
+        finish = resolve;
+      }),
+  );
+  return {
+    finish: () => finish(),
+  };
+}
+
 describe("relay external socket reconnect behavior", () => {
   beforeEach(() => {
     sessionMock.instances.length = 0;
@@ -517,6 +532,36 @@ describe("relay external socket reconnect behavior", () => {
     await server.close();
   });
 
+  test("rejects sockets attached after shutdown begins", async () => {
+    const server = createServer();
+    const existingSocket = new MockSocket();
+    await attachRelayAndHello({
+      server,
+      socket: existingSocket,
+      clientId: "existing-client",
+    });
+
+    const heldCleanup = holdSessionCleanup(sessionMock.instances[0]);
+    const closePromise = server.close();
+
+    const lateSocket = new MockSocket();
+    try {
+      await server.attachExternalSocket(lateSocket, { transport: "relay" });
+      lateSocket.emit("message", JSON.stringify(createHelloMessage("late-client")));
+
+      expect({
+        readyState: lateSocket.readyState,
+        sessionCount: sessionMock.instances.length,
+      }).toEqual({
+        readyState: 3,
+        sessionCount: 1,
+      });
+    } finally {
+      heldCleanup.finish();
+      await closePromise;
+    }
+  });
+
   test("closes pending connection when hello timeout elapses", async () => {
     const server = createServer();
 
diff --git a/packages/server/src/server/websocket-server.ts b/packages/server/src/server/websocket-server.ts
index 3c2143b9b..5b45cf7a3 100644
--- a/packages/server/src/server/websocket-server.ts
+++ b/packages/server/src/server/websocket-server.ts
@@ -351,6 +351,7 @@ const HELLO_TIMEOUT_MS = 15_000;
 const WS_CLOSE_HELLO_TIMEOUT = 4001;
 const WS_CLOSE_INVALID_HELLO = 4002;
 const WS_CLOSE_INCOMPATIBLE_PROTOCOL = 4003;
+const WS_CLOSE_SERVER_SHUTDOWN = 1001;
 const WS_PROTOCOL_VERSION = 1;
 const WS_RUNTIME_METRICS_FLUSH_MS = 30_000;
 
@@ -463,6 +464,7 @@ export class VoiceAssistantWebSocketServer {
   private unsubscribeTerminalActivity: (() => void) | null = null;
   private readonly browserToolsBroker: BrowserToolsBroker | null;
   private readonly browserToolsRegistrations = new Map<string, BrowserToolsRegistration>();
+  private acceptingConnections = true;
 
   constructor(
     server: HTTPServer,
@@ -708,6 +710,11 @@ export class VoiceAssistantWebSocketServer {
     hostnames: HostnamesConfig | undefined,
     callback: (res: boolean, code?: number, message?: string) => void,
   ): void {
+    if (!this.acceptingConnections) {
+      callback(false, 503, "Server shutting down");
+      return;
+    }
+
     const requestMetadata = extractSocketRequestMetadata(req);
     const origin = requestMetadata.origin;
     const requestHost = requestMetadata.host ?? null;
@@ -799,7 +806,12 @@ export class VoiceAssistantWebSocketServer {
     await this.attachSocket(ws, undefined, metadata);
   }
 
+  public prepareForShutdown(): void {
+    this.acceptingConnections = false;
+  }
+
   public async close(): Promise<void> {
+    this.prepareForShutdown();
     this.unsubscribeSpeechReadiness?.();
     this.unsubscribeSpeechReadiness = null;
     this.unsubscribeDaemonConfigChange?.();
@@ -921,6 +933,15 @@ export class VoiceAssistantWebSocketServer {
     request?: unknown,
     metadata?: ExternalSocketMetadata,
   ): Promise<void> {
+    if (!this.acceptingConnections) {
+      try {
+        ws.close(WS_CLOSE_SERVER_SHUTDOWN, "Server shutting down");
+      } catch {
+        // ignore close errors
+      }
+      return;
+    }
+
     const requestMetadata = extractSocketRequestMetadata(request);
     const identity = createWebSocketConnectionIdentity(requestMetadata, metadata);
     this.socketIdentities.set(ws, identity);
@@ -1609,6 +1630,10 @@ export class VoiceAssistantWebSocketServer {
     ws: WebSocketLike,
     data: Buffer | ArrayBuffer | Buffer[] | string,
   ): void {
+    if (!this.acceptingConnections) {
+      return;
+    }
+
     const activeConnection = this.sessions.get(ws);
     const pendingConnection = this.pendingConnections.get(ws);
     const log =