diff --git a/packages/server/src/server/agent/agent-manager.test.ts b/packages/server/src/server/agent/agent-manager.test.ts
index d7302ef77..277fffe69 100644
--- a/packages/server/src/server/agent/agent-manager.test.ts
+++ b/packages/server/src/server/agent/agent-manager.test.ts
@@ -9,6 +9,7 @@ import { AgentManager } from "./agent-manager.js";
 import { AgentStorage } from "./agent-storage.js";
 import type {
   AgentClient,
+  AgentPersistenceHandle,
   AgentRunResult,
   AgentSession,
   AgentSessionConfig,
@@ -149,6 +150,99 @@ describe("AgentManager", () => {
     ).rejects.toThrow("Working directory does not exist");
   });
 
+  test("resumeAgent keeps metadata config and applies systemPrompt/mcpServers overrides", async () => {
+    const workdir = mkdtempSync(join(tmpdir(), "agent-manager-resume-"));
+    const storagePath = join(workdir, "agents");
+    const storage = new AgentStorage(storagePath, logger);
+
+    class ResumeCaptureClient implements AgentClient {
+      readonly provider = "codex" as const;
+      readonly capabilities = TEST_CAPABILITIES;
+      lastResumeOverrides: Partial<AgentSessionConfig> | undefined;
+
+      async isAvailable(): Promise<boolean> {
+        return true;
+      }
+
+      async createSession(config: AgentSessionConfig): Promise<AgentSession> {
+        return new TestAgentSession(config);
+      }
+
+      async resumeSession(
+        handle: AgentPersistenceHandle,
+        overrides?: Partial<AgentSessionConfig>
+      ): Promise<AgentSession> {
+        this.lastResumeOverrides = overrides;
+        const metadata = (handle.metadata ?? {}) as Partial<AgentSessionConfig>;
+        const merged: AgentSessionConfig = {
+          ...metadata,
+          ...overrides,
+          provider: "codex",
+          cwd: overrides?.cwd ?? metadata.cwd ?? process.cwd(),
+        };
+        return new TestAgentSession(merged);
+      }
+    }
+
+    const client = new ResumeCaptureClient();
+    const manager = new AgentManager({
+      clients: {
+        codex: client,
+      },
+      registry: storage,
+      logger,
+      idFactory: () => "00000000-0000-4000-8000-000000000106",
+    });
+
+    const handle: AgentPersistenceHandle = {
+      provider: "codex",
+      sessionId: "resume-session-1",
+      metadata: {
+        provider: "codex",
+        cwd: workdir,
+        systemPrompt: "old prompt",
+        mcpServers: {
+          legacy: {
+            type: "stdio",
+            command: "legacy-bridge",
+            args: ["/tmp/legacy.sock"],
+          },
+        },
+      },
+    };
+
+    const resumed = await manager.resumeAgent(handle, {
+      cwd: workdir,
+      systemPrompt: "new prompt",
+      mcpServers: {
+        paseo: {
+          type: "stdio",
+          command: "node",
+          args: ["/tmp/mcp-bridge.mjs", "--socket", "/tmp/paseo.sock"],
+        },
+      },
+    });
+
+    expect(resumed.config.systemPrompt).toBe("new prompt");
+    expect(resumed.config.mcpServers).toEqual({
+      paseo: {
+        type: "stdio",
+        command: "node",
+        args: ["/tmp/mcp-bridge.mjs", "--socket", "/tmp/paseo.sock"],
+      },
+    });
+    expect(client.lastResumeOverrides).toMatchObject({
+      systemPrompt: "new prompt",
+      mcpServers: {
+        paseo: {
+          type: "stdio",
+          command: "node",
+          args: ["/tmp/mcp-bridge.mjs", "--socket", "/tmp/paseo.sock"],
+        },
+      },
+    });
+  });
+
   test("createAgent fails when generated agent ID is not a UUID", async () => {
     const workdir = mkdtempSync(join(tmpdir(), "agent-manager-test-"));
     const storagePath = join(workdir, "agents");
diff --git a/packages/server/src/server/agent/agent-projections.ts b/packages/server/src/server/agent/agent-projections.ts
index e12f5c2c0..542bbf766 100644
--- a/packages/server/src/server/agent/agent-projections.ts
+++ b/packages/server/src/server/agent/agent-projections.ts
@@ -129,6 +129,9 @@ function buildSerializableConfig(
   if (extra !== undefined) {
     serializable.extra = extra;
   }
+  if (config.systemPrompt) {
+    serializable.systemPrompt = config.systemPrompt;
+  }
   if (config.mcpServers) {
     serializable.mcpServers = config.mcpServers;
   }
diff --git a/packages/server/src/server/agent/agent-storage.test.ts b/packages/server/src/server/agent/agent-storage.test.ts
index 4b0004d37..c3868167c 100644
--- a/packages/server/src/server/agent/agent-storage.test.ts
+++ b/packages/server/src/server/agent/agent-storage.test.ts
@@ -39,6 +39,7 @@ function createManagedAgent(
     modeId: configOverrides.modeId ?? "plan",
     model: configOverrides.model ?? "gpt-5.1",
     extra: configOverrides.extra ?? { claude: { maxThinkingTokens: 1024 } },
+    systemPrompt: configOverrides.systemPrompt,
     mcpServers: configOverrides.mcpServers,
   };
   const session =
@@ -119,6 +120,7 @@ describe("AgentStorage", () => {
         config: {
           modeId: "coding",
           model: "gpt-5.1",
+          systemPrompt: "Be terse and explicit.",
           extra: { claude: { maxThinkingTokens: 1024 } },
           mcpServers: {
             paseo: {
@@ -137,6 +139,7 @@ describe("AgentStorage", () => {
     expect(record.provider).toBe("claude");
     expect(record.config?.modeId).toBe("coding");
     expect(record.config?.model).toBe("gpt-5.1");
+    expect(record.config?.systemPrompt).toBe("Be terse and explicit.");
     expect(record.config?.mcpServers).toEqual({
       paseo: {
         type: "stdio",
diff --git a/packages/server/src/server/agent/agent-storage.ts b/packages/server/src/server/agent/agent-storage.ts
index 0af305865..94f9e1462 100644
--- a/packages/server/src/server/agent/agent-storage.ts
+++ b/packages/server/src/server/agent/agent-storage.ts
@@ -15,6 +15,7 @@ const SERIALIZABLE_CONFIG_SCHEMA = z
     model: z.string().nullable().optional(),
     thinkingOptionId: z.string().nullable().optional(),
     extra: z.record(z.any()).nullable().optional(),
+    systemPrompt: z.string().nullable().optional(),
     mcpServers: z.record(z.any()).nullable().optional(),
   })
   .nullable()
@@ -62,7 +63,7 @@ const STORED_AGENT_SCHEMA = z.object({
 
 export type SerializableAgentConfig = Pick<
   AgentSessionConfig,
-  "modeId" | "model" | "thinkingOptionId" | "extra" | "mcpServers"
+  "modeId" | "model" | "thinkingOptionId" | "extra" | "systemPrompt" | "mcpServers"
 >;
 
 export type StoredAgentRecord = z.infer<typeof STORED_AGENT_SCHEMA>;
diff --git a/packages/server/src/server/agent/providers/claude-agent.ts b/packages/server/src/server/agent/providers/claude-agent.ts
index c259712da..7e8608f2e 100644
--- a/packages/server/src/server/agent/providers/claude-agent.ts
+++ b/packages/server/src/server/agent/providers/claude-agent.ts
@@ -270,6 +270,9 @@ function coerceSessionMetadata(metadata: AgentMetadata | undefined): Partial<Age
       result.extra = extra;
     }
   }
+  if (typeof metadata.systemPrompt === "string") {
+    result.systemPrompt = metadata.systemPrompt;
+  }
   if (isMcpServersRecord(metadata.mcpServers)) {
     result.mcpServers = metadata.mcpServers;
   }
diff --git a/packages/server/src/server/agent/providers/codex-app-server-agent.ts b/packages/server/src/server/agent/providers/codex-app-server-agent.ts
index ddf44bd5c..b9b1f8eb8 100644
--- a/packages/server/src/server/agent/providers/codex-app-server-agent.ts
+++ b/packages/server/src/server/agent/providers/codex-app-server-agent.ts
@@ -1597,6 +1597,9 @@ class CodexAppServerAgentSession implements AgentSession {
         modeId: this.currentMode,
         model: this.config.model ?? null,
         thinkingOptionId,
+        extra: this.config.extra,
+        systemPrompt: this.config.systemPrompt,
+        mcpServers: this.config.mcpServers,
       },
     };
   }
diff --git a/packages/server/src/server/agent/providers/codex-mcp-agent.ts b/packages/server/src/server/agent/providers/codex-mcp-agent.ts
index 85be3bd85..9371a379e 100644
--- a/packages/server/src/server/agent/providers/codex-mcp-agent.ts
+++ b/packages/server/src/server/agent/providers/codex-mcp-agent.ts
@@ -1961,6 +1961,7 @@ const AgentSessionConfigSchema = z
     networkAccess: z.boolean().optional(),
     webSearch: z.boolean().optional(),
     extra: AgentSessionExtraSchema.optional(),
+    systemPrompt: z.string().optional(),
     mcpServers: z.record(McpServerConfigSchema).optional(),
   })
   .passthrough();
diff --git a/packages/server/src/server/persistence-hooks.test.ts b/packages/server/src/server/persistence-hooks.test.ts
index 0a601eabd..a7b3aa819 100644
--- a/packages/server/src/server/persistence-hooks.test.ts
+++ b/packages/server/src/server/persistence-hooks.test.ts
@@ -4,6 +4,8 @@ import type { ManagedAgent } from "./agent/agent-manager.js";
 import type { StoredAgentRecord } from "./agent/agent-storage.js";
 import {
   attachAgentStoragePersistence,
+  buildConfigOverrides,
+  buildSessionConfig,
 } from "./persistence-hooks.js";
 import type {
   AgentPermissionRequest,
@@ -140,4 +142,72 @@ describe("persistence hooks", () => {
     });
     expect(applySnapshot).toHaveBeenCalledTimes(1);
   });
+
+  test("buildConfigOverrides carries systemPrompt and mcpServers", () => {
+    const record = createRecord({
+      title: "Voice agent",
+      config: {
+        modeId: "default",
+        model: "gpt-5.1-codex-mini",
+        thinkingOptionId: "minimal",
+        systemPrompt: "Use speak first.",
+        mcpServers: {
+          paseo: {
+            type: "stdio",
+            command: "node",
+            args: ["/tmp/bridge.mjs", "--socket", "/tmp/agent.sock"],
+          },
+        },
+      },
+    });
+
+    expect(buildConfigOverrides(record)).toMatchObject({
+      cwd: "/tmp/project",
+      modeId: "plan",
+      model: "gpt-5.1-codex-mini",
+      thinkingOptionId: "minimal",
+      title: "Voice agent",
+      systemPrompt: "Use speak first.",
+      mcpServers: {
+        paseo: {
+          type: "stdio",
+          command: "node",
+          args: ["/tmp/bridge.mjs", "--socket", "/tmp/agent.sock"],
+        },
+      },
+    });
+  });
+
+  test("buildSessionConfig includes persisted systemPrompt and mcpServers", () => {
+    const record = createRecord({
+      provider: "codex",
+      config: {
+        modeId: "default",
+        model: "gpt-5.1-codex-mini",
+        systemPrompt: "Confirm and speak first.",
+        mcpServers: {
+          paseo: {
+            type: "stdio",
+            command: "node",
+            args: ["/tmp/bridge.mjs", "--socket", "/tmp/agent.sock"],
+          },
+        },
+      },
+    });
+
+    expect(buildSessionConfig(record)).toMatchObject({
+      provider: "codex",
+      cwd: "/tmp/project",
+      modeId: "plan",
+      model: "gpt-5.1-codex-mini",
+      systemPrompt: "Confirm and speak first.",
+      mcpServers: {
+        paseo: {
+          type: "stdio",
+          command: "node",
+          args: ["/tmp/bridge.mjs", "--socket", "/tmp/agent.sock"],
+        },
+      },
+    });
+  });
 });
diff --git a/packages/server/src/server/persistence-hooks.ts b/packages/server/src/server/persistence-hooks.ts
index dc5a3b2ae..7f56e6841 100644
--- a/packages/server/src/server/persistence-hooks.ts
+++ b/packages/server/src/server/persistence-hooks.ts
@@ -56,6 +56,7 @@ export function buildConfigOverrides(
     thinkingOptionId: record.config?.thinkingOptionId ?? undefined,
     title: record.title ?? undefined,
     extra: record.config?.extra ?? undefined,
+    systemPrompt: record.config?.systemPrompt ?? undefined,
     mcpServers: record.config?.mcpServers ?? undefined,
   };
 }
@@ -75,6 +76,7 @@ export function buildSessionConfig(
     thinkingOptionId: overrides.thinkingOptionId,
     title: overrides.title,
     extra: overrides.extra,
+    systemPrompt: overrides.systemPrompt,
     mcpServers: overrides.mcpServers,
   };
 }
diff --git a/packages/server/src/shared/messages.ts b/packages/server/src/shared/messages.ts
index 9acfcb49b..15a7c8eb7 100644
--- a/packages/server/src/shared/messages.ts
+++ b/packages/server/src/shared/messages.ts
@@ -105,6 +105,7 @@ const AgentSessionConfigSchema = z.object({
     })
     .partial()
     .optional(),
+  systemPrompt: z.string().optional(),
   mcpServers: z.record(McpServerConfigSchema).optional(),
 });