diff --git a/packages/server/src/server/agent/agent-manager.test.ts b/packages/server/src/server/agent/agent-manager.test.ts
index 1d6f323deb..fd28fe5550 100644
--- a/packages/server/src/server/agent/agent-manager.test.ts
+++ b/packages/server/src/server/agent/agent-manager.test.ts
@@ -956,6 +956,73 @@ test("unavailable steer interrupts once and starts one replacement turn", async
   }
 });
 
+test("steers a send that arrives while the previous turn is still starting", async () => {
+  const startHeld = deferred<void>();
+  class SlowStartSteeringSession extends SteeringTestSession {
+    override async startTurn(prompt: AgentPromptInput): Promise<{ turnId: string }> {
+      await startHeld.promise;
+      return await super.startTurn(prompt);
+    }
+  }
+  const session = new SlowStartSteeringSession({
+    provider: "codex",
+    cwd: process.cwd(),
+  });
+  const workdir = mkdtempSync(join(tmpdir(), "agent-manager-steer-starting-"));
+  const manager = new AgentManager({
+    clients: {
+      codex: new (class extends TestAgentClient {
+        override async createSession(): Promise<AgentSession> {
+          return session;
+        }
+      })(),
+    },
+    logger,
+  });
+  let agentId: string | null = null;
+  try {
+    const agent = await manager.createAgent({ provider: "codex", cwd: workdir }, undefined, {
+      workspaceId: undefined,
+    });
+    agentId = agent.id;
+    const steerOptions = (clientMessageId: string) => ({
+      replaceRunning: true,
+      activeTurnBehavior: "steer" as const,
+      runOptions: { clientMessageId },
+    });
+    await startAgentRun(manager, agent.id, "FIRST", logger, steerOptions("first-client"));
+    const second = startAgentRun(
+      manager,
+      agent.id,
+      "SECOND",
+      logger,
+      steerOptions("second-client"),
+    );
+
+    startHeld.resolve();
+    await expect(second).resolves.toEqual({ disposition: "steered" });
+
+    expect(session.startPrompts).toEqual(["FIRST"]);
+    expect(session.interruptCount).toBe(0);
+    expect(
+      manager
+        .fetchTimeline(agent.id, { limit: 0 })
+        .rows.filter((row) => row.item.type === "user_message")
+        .map((row) => ({
+          text: row.item.type === "user_message" ? row.item.text : null,
+          turnId: row.turnId,
+        })),
+    ).toEqual([
+      { text: "FIRST", turnId: "active-turn-1" },
+      { text: "SECOND", turnId: "active-turn-1" },
+    ]);
+  } finally {
+    startHeld.resolve();
+    if (agentId) await manager.closeAgent(agentId).catch(() => undefined);
+    rmSync(workdir, { recursive: true, force: true });
+  }
+});
+
 test("orders an accepted steer before output emitted while acknowledgement is pending", async () => {
   const entered = deferred<void>();
   const release = deferred<void>();
diff --git a/packages/server/src/server/agent/agent-manager.ts b/packages/server/src/server/agent/agent-manager.ts
index 46c822ea2d..a89eb338b7 100644
--- a/packages/server/src/server/agent/agent-manager.ts
+++ b/packages/server/src/server/agent/agent-manager.ts
@@ -2734,7 +2734,7 @@ export class AgentManager {
         throw error;
       }
       if (isStaleProviderSessionError(error)) {
-        pendingRun.start = { status: "failed", error: error.message };
+        this.runs.settleForegroundStart(pendingRun, { status: "failed", error: error.message });
         agent.pendingReplacement = false;
         if (!agent.activeForegroundTurnId) agent.lifecycle = "idle";
         this.runs.settleForegroundRun(agentId, pendingRun.token);
@@ -2742,7 +2742,7 @@ export class AgentManager {
       }
       agent.pendingReplacement = false;
       const errorMsg = error instanceof Error ? error.message : "Failed to start turn";
-      pendingRun.start = { status: "failed", error: errorMsg };
+      this.runs.settleForegroundStart(pendingRun, { status: "failed", error: errorMsg });
       // A terminal rejection belongs after the submitted prompt even though no provider turn exists.
       if (options?.clientMessageId) {
         this.recordSubmittedPrompt(agent, prompt, options.clientMessageId, "rejected", {
@@ -2832,7 +2832,7 @@ export class AgentManager {
         agent.pendingReplacement = false;
       }
       const turnStartedAt = new Date();
-      pendingRun.start = { status: "started", turnId };
+      this.runs.settleForegroundStart(pendingRun, { status: "started", turnId });
       agent.activeForegroundTurnId = turnId;
       this.openActiveTurn(agent, turnId, turnStartedAt);
       agent.lifecycle = "running";
@@ -3041,6 +3041,9 @@ export class AgentManager {
     prompt: AgentPromptInput,
     options?: AgentSteerOptions,
   ): Promise<ActiveTurnSteerDispatchResult> {
+    // A turn that is still starting has no id to steer yet. Replacing it would drop its
+    // prompt, so wait until it is accepted (or fails) and steer the turn it became.
+    await this.runs.waitForForegroundStart(agentId);
     const agent = this.requireSessionAgent(agentId);
     const expectedTurnId = agent.activeForegroundTurnId ?? agent.activeTurnId;
     if (!expectedTurnId) {
diff --git a/packages/server/src/server/agent/agent-run-state.ts b/packages/server/src/server/agent/agent-run-state.ts
index ad1eb0af34..f2f4ee3d16 100644
--- a/packages/server/src/server/agent/agent-run-state.ts
+++ b/packages/server/src/server/agent/agent-run-state.ts
@@ -10,14 +10,18 @@ export interface ForegroundTurnWaiter {
   resolveSettled: () => void;
 }
 
+type ForegroundRunStart =
+  | { status: "pending" }
+  | { status: "started"; turnId: string }
+  | { status: "failed"; error: string };
+
 export interface PendingForegroundRun {
   token: string;
   kind: "foreground";
   stagedEvents: AgentStreamEvent[];
-  start:
-    | { status: "pending" }
-    | { status: "started"; turnId: string }
-    | { status: "failed"; error: string };
+  start: ForegroundRunStart;
+  startSettledPromise: Promise<void>;
+  resolveStartSettled: () => void;
   settled: boolean;
   settledPromise: Promise<void>;
   resolveSettled: () => void;
@@ -54,6 +58,23 @@ export class AgentRunState {
     return run?.kind === "foreground" ? run : null;
   }
 
+  settleForegroundStart(
+    run: PendingForegroundRun,
+    start: Exclude<ForegroundRunStart, { status: "pending" }>,
+  ): void {
+    run.start = start;
+    run.resolveStartSettled();
+  }
+
+  /** Resolves once the agent's foreground run has a turn id, failed to start, or ended. */
+  async waitForForegroundStart(agentId: string): Promise<void> {
+    const run = this.getPendingRun(agentId);
+    if (run?.start.status !== "pending") {
+      return;
+    }
+    await Promise.race([run.startSettledPromise, run.settledPromise]);
+  }
+
   hasPendingRun(agentId: string): boolean {
     return this.getPendingRun(agentId) !== null;
   }
@@ -277,10 +298,16 @@ export class ForegroundTurnStream {
 }
 
 function createPendingForegroundRun(): PendingForegroundRun {
+  let resolveStartSettled!: () => void;
+  const startSettledPromise = new Promise<void>((resolvePromise) => {
+    resolveStartSettled = resolvePromise;
+  });
   return {
     ...createTrackedRunState(),
     kind: "foreground",
     start: { status: "pending" },
+    startSettledPromise,
+    resolveStartSettled,
     stagedEvents: [],
   };
 }