diff --git a/src/agents/embedded-agent-runner/run/attempt-stream-runtime-prepare.test.ts b/src/agents/embedded-agent-runner/run/attempt-stream-runtime-prepare.test.ts
index 73195aa139f3..28f6ce50e08d 100644
--- a/src/agents/embedded-agent-runner/run/attempt-stream-runtime-prepare.test.ts
+++ b/src/agents/embedded-agent-runner/run/attempt-stream-runtime-prepare.test.ts
@@ -228,6 +228,25 @@ describe("prepareEmbeddedAttemptStreamRuntime", () => {
     expect(mocks.withOwnedSessionTranscriptWrites).toHaveBeenCalledOnce();
   });
 
+  it.each([
+    { label: "external cancellation", message: "run cancelled" },
+    { label: "run timeout", message: "run timed out" },
+  ])("does not start a prompt after $label", async ({ message }) => {
+    const fixture = createFixture();
+    const runtime = await prepareEmbeddedAttemptStreamRuntime(fixture.input);
+    const reason = new Error(message);
+    const abortError = new Error(message, { cause: reason });
+    abortError.name = "AbortError";
+    fixture.input.runAbortController.abort(reason);
+    mocks.abortable.mockImplementationOnce((_signal, _promise) => Promise.reject(abortError));
+
+    await expect(runtime.promptActiveSession("must not start")).rejects.toBe(abortError);
+
+    expect(fixture.activeSession.prompt).not.toHaveBeenCalled();
+    expect(fixture.trackPromptSettlePromise).not.toHaveBeenCalled();
+    expect(mocks.abortable).toHaveBeenCalledOnce();
+  });
+
   it("flushes pending tool results and disposes the session when history preparation fails", async () => {
     const fixture = createFixture({ aborted: true });
     const failure = new Error("history failed");
diff --git a/src/agents/embedded-agent-runner/run/attempt-stream-runtime-prepare.ts b/src/agents/embedded-agent-runner/run/attempt-stream-runtime-prepare.ts
index edcfe89e09bf..3458e5ff8ed1 100644
--- a/src/agents/embedded-agent-runner/run/attempt-stream-runtime-prepare.ts
+++ b/src/agents/embedded-agent-runner/run/attempt-stream-runtime-prepare.ts
@@ -137,9 +137,14 @@ export async function prepareEmbeddedAttemptStreamRuntime(input: {
     prompt: string,
     options?: Parameters<typeof activeSession.prompt>[1],
   ): Promise<void> =>
-    withOwnedSessionTranscriptWrites(input.ownedTranscriptWriteContext, async () =>
-      abortable(input.trackPromptSettlePromise(activeSession.prompt(prompt, options))),
-    );
+    withOwnedSessionTranscriptWrites(input.ownedTranscriptWriteContext, async () => {
+      // Prompting starts its own agent loop; reject before creating a loop that
+      // an already-aborted attempt can no longer cancel.
+      if (input.runAbortController.signal.aborted) {
+        return abortable(Promise.resolve());
+      }
+      return abortable(input.trackPromptSettlePromise(activeSession.prompt(prompt, options)));
+    });
   const onBlockReply = attempt.onBlockReply
     ? bindOwnedSessionTranscriptWrites(input.ownedTranscriptWriteContext, attempt.onBlockReply)
     : undefined;