diff --git a/packages/server/src/server/agent/agent-manager.test.ts b/packages/server/src/server/agent/agent-manager.test.ts
index c9d0ebce73..11339a729c 100644
--- a/packages/server/src/server/agent/agent-manager.test.ts
+++ b/packages/server/src/server/agent/agent-manager.test.ts
@@ -957,6 +957,64 @@ test("steers a send that arrives while the previous turn is still starting", asy
   }
 });
 
+test("starts its own turn when the previous turn fails to start under a steer send", async () => {
+  const startHeld = deferred<void>();
+  class FailingFirstStartSession extends SteeringTestSession {
+    override async startTurn(prompt: AgentPromptInput): Promise<{ turnId: string }> {
+      if (prompt === "FIRST") {
+        this.startPrompts.push(prompt);
+        await startHeld.promise;
+        throw new Error("first start failed");
+      }
+      return await super.startTurn(prompt);
+    }
+  }
+  const session = new FailingFirstStartSession({
+    provider: "codex",
+    cwd: process.cwd(),
+  });
+  const workdir = mkdtempSync(join(tmpdir(), "agent-manager-steer-failed-start-"));
+  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: "turn_started" });
+    await vi.waitFor(() => expect(session.startPrompts).toEqual(["FIRST", "SECOND"]));
+    expect(session.interruptCount).toBe(0);
+  } 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-run-state.ts b/packages/server/src/server/agent/agent-run-state.ts
index f2f4ee3d16..0ea85f6d81 100644
--- a/packages/server/src/server/agent/agent-run-state.ts
+++ b/packages/server/src/server/agent/agent-run-state.ts
@@ -20,8 +20,8 @@ export interface PendingForegroundRun {
   kind: "foreground";
   stagedEvents: AgentStreamEvent[];
   start: ForegroundRunStart;
-  startSettledPromise: Promise<void>;
-  resolveStartSettled: () => void;
+  turnStartedPromise: Promise<void>;
+  resolveTurnStarted: () => void;
   settled: boolean;
   settledPromise: Promise<void>;
   resolveSettled: () => void;
@@ -63,16 +63,21 @@ export class AgentRunState {
     start: Exclude<ForegroundRunStart, { status: "pending" }>,
   ): void {
     run.start = start;
-    run.resolveStartSettled();
+    if (start.status === "started") {
+      run.resolveTurnStarted();
+    }
   }
 
-  /** Resolves once the agent's foreground run has a turn id, failed to start, or ended. */
+  /**
+   * Resolves once the agent's foreground run has a turn id or has ended. A failed start
+   * resolves only once its run is cleared, so callers never see a failed run still tracked.
+   */
   async waitForForegroundStart(agentId: string): Promise<void> {
     const run = this.getPendingRun(agentId);
     if (run?.start.status !== "pending") {
       return;
     }
-    await Promise.race([run.startSettledPromise, run.settledPromise]);
+    await Promise.race([run.turnStartedPromise, run.settledPromise]);
   }
 
   hasPendingRun(agentId: string): boolean {
@@ -298,16 +303,16 @@ export class ForegroundTurnStream {
 }
 
 function createPendingForegroundRun(): PendingForegroundRun {
-  let resolveStartSettled!: () => void;
-  const startSettledPromise = new Promise<void>((resolvePromise) => {
-    resolveStartSettled = resolvePromise;
+  let resolveTurnStarted!: () => void;
+  const turnStartedPromise = new Promise<void>((resolvePromise) => {
+    resolveTurnStarted = resolvePromise;
   });
   return {
     ...createTrackedRunState(),
     kind: "foreground",
     start: { status: "pending" },
-    startSettledPromise,
-    resolveStartSettled,
+    turnStartedPromise,
+    resolveTurnStarted,
     stagedEvents: [],
   };
 }