diff --git a/src/agents/embedded-agent-runner/run.prompt-timeout-fallback.test.ts b/src/agents/embedded-agent-runner/run.prompt-timeout-fallback.test.ts
new file mode 100644
index 000000000000..812a83fdd86c
--- /dev/null
+++ b/src/agents/embedded-agent-runner/run.prompt-timeout-fallback.test.ts
@@ -0,0 +1,99 @@
+// Coverage for handing replay-safe plugin-harness prompt timeouts to model fallback.
+import { beforeAll, beforeEach, describe, expect, it } from "vitest";
+import { makeModelFallbackCfg } from "../test-helpers/model-fallback-config-fixture.js";
+import { makeAttemptResult } from "./run.overflow-compaction.fixture.js";
+import {
+  loadRunOverflowCompactionHarness,
+  MockedFailoverError,
+  mockedClassifyFailoverReason,
+  mockedRunEmbeddedAttempt,
+  overflowBaseRunParams,
+  resetRunOverflowCompactionHarnessMocks,
+} from "./run.overflow-compaction.harness.js";
+
+let runEmbeddedAgent: typeof import("./run.js").runEmbeddedAgent;
+
+describe("runEmbeddedAgent prompt timeout fallback handoff", () => {
+  beforeAll(async () => {
+    ({ runEmbeddedAgent } = await loadRunOverflowCompactionHarness());
+  });
+
+  beforeEach(() => {
+    resetRunOverflowCompactionHarnessMocks();
+  });
+
+  it("throws FailoverError for replay-safe harness-owned prompt timeouts when model fallbacks are configured", async () => {
+    mockedClassifyFailoverReason.mockReturnValue("timeout");
+    mockedRunEmbeddedAttempt.mockResolvedValueOnce(
+      makeAttemptResult({
+        assistantTexts: [],
+        promptError: new Error("LLM request timed out."),
+        promptErrorSource: "prompt",
+      }),
+    );
+
+    const promise = runEmbeddedAgent({
+      ...overflowBaseRunParams,
+      provider: "openai",
+      model: "gpt-5.4",
+      runId: "run-prompt-timeout-fallback",
+      config: makeModelFallbackCfg({
+        agents: {
+          defaults: {
+            model: {
+              primary: "openai/gpt-5.4",
+              fallbacks: ["anthropic/claude-opus-4-6"],
+            },
+          },
+        },
+      }),
+    });
+
+    await expect(promise).rejects.toBeInstanceOf(MockedFailoverError);
+    await expect(promise).rejects.toThrow("LLM request timed out.");
+    expect(mockedRunEmbeddedAttempt).toHaveBeenCalledTimes(1);
+  });
+
+  it("surfaces replay-invalid prompt timeouts instead of handing them to model fallback", async () => {
+    mockedClassifyFailoverReason.mockReturnValue("timeout");
+    mockedRunEmbeddedAttempt.mockResolvedValueOnce(
+      makeAttemptResult({
+        assistantTexts: [],
+        promptError: new Error("LLM request timed out."),
+        promptErrorSource: "prompt",
+        promptTimeoutOutcome: {
+          message: "Harness abandoned the timed-out turn after provider activity.",
+          replayInvalid: true,
+          livenessState: "abandoned",
+        },
+      }),
+    );
+
+    let thrown: unknown;
+    try {
+      await runEmbeddedAgent({
+        ...overflowBaseRunParams,
+        provider: "openai",
+        model: "gpt-5.4",
+        runId: "run-prompt-timeout-replay-invalid",
+        config: makeModelFallbackCfg({
+          agents: {
+            defaults: {
+              model: {
+                primary: "openai/gpt-5.4",
+                fallbacks: ["anthropic/claude-opus-4-6"],
+              },
+            },
+          },
+        }),
+      });
+    } catch (err) {
+      thrown = err;
+    }
+
+    expect(thrown).toBeInstanceOf(Error);
+    expect(thrown).not.toBeInstanceOf(MockedFailoverError);
+    expect(String((thrown as Error | undefined)?.message)).toContain("LLM request timed out.");
+    expect(mockedRunEmbeddedAttempt).toHaveBeenCalledTimes(1);
+  });
+});
diff --git a/src/agents/embedded-agent-runner/run.ts b/src/agents/embedded-agent-runner/run.ts
index 7c7468ce3d17..9e7e95905ff1 100644
--- a/src/agents/embedded-agent-runner/run.ts
+++ b/src/agents/embedded-agent-runner/run.ts
@@ -3116,6 +3116,12 @@ async function runEmbeddedAgentInternal(
             );
             const promptFailoverFailure =
               promptFailoverReason !== null || isFailoverErrorMessage(errorText, { provider });
+            const promptTimeoutFallbackSafe =
+              promptErrorSource === "prompt" &&
+              promptFailoverReason === "timeout" &&
+              !attempt.codexAppServerFailure &&
+              attempt.promptTimeoutOutcome?.replayInvalid !== true &&
+              attempt.replayMetadata.replaySafe;
             // Capture the failing profile before auth-profile rotation mutates `lastProfileId`.
             const failedPromptProfileId = lastProfileId;
             const logPromptFailoverDecision = createFailoverDecisionLogger({
@@ -3147,6 +3153,7 @@ async function runEmbeddedAgentInternal(
               failoverFailure: promptFailoverFailure,
               failoverReason: promptFailoverReason,
               harnessOwnsTransport: pluginHarnessOwnsTransport,
+              promptTimeoutFallbackSafe,
               profileRotated: false,
             });
             if (
@@ -3186,6 +3193,7 @@ async function runEmbeddedAgentInternal(
                 failoverFailure: promptFailoverFailure,
                 failoverReason: promptFailoverReason,
                 harnessOwnsTransport: pluginHarnessOwnsTransport,
+                promptTimeoutFallbackSafe,
                 profileRotated: true,
               });
             }
diff --git a/src/agents/embedded-agent-runner/run/failover-policy.test.ts b/src/agents/embedded-agent-runner/run/failover-policy.test.ts
index fe2f8caac089..7f773f7701b0 100644
--- a/src/agents/embedded-agent-runner/run/failover-policy.test.ts
+++ b/src/agents/embedded-agent-runner/run/failover-policy.test.ts
@@ -581,6 +581,44 @@ describe("resolveRunFailoverDecision", () => {
     });
   });
 
+  it("falls back on fallback-safe harness-owned prompt timeouts", () => {
+    expect(
+      resolveRunFailoverDecision({
+        stage: "prompt",
+        aborted: false,
+        externalAbort: false,
+        fallbackConfigured: true,
+        failoverFailure: true,
+        failoverReason: "timeout",
+        harnessOwnsTransport: true,
+        promptTimeoutFallbackSafe: true,
+        profileRotated: true,
+      }),
+    ).toEqual({
+      action: "fallback_model",
+      reason: "timeout",
+    });
+  });
+
+  it("surfaces fallback-safe harness-owned prompt timeouts when no fallback is configured", () => {
+    expect(
+      resolveRunFailoverDecision({
+        stage: "prompt",
+        aborted: false,
+        externalAbort: false,
+        fallbackConfigured: false,
+        failoverFailure: true,
+        failoverReason: "timeout",
+        harnessOwnsTransport: true,
+        promptTimeoutFallbackSafe: true,
+        profileRotated: true,
+      }),
+    ).toEqual({
+      action: "surface_error",
+      reason: "timeout",
+    });
+  });
+
   it("surfaces error on LLM idle timeout when no fallback is configured and rotation is exhausted", () => {
     expect(
       resolveRunFailoverDecision({
diff --git a/src/agents/embedded-agent-runner/run/failover-policy.ts b/src/agents/embedded-agent-runner/run/failover-policy.ts
index c1a1a23c2df2..f91ee89f81f7 100644
--- a/src/agents/embedded-agent-runner/run/failover-policy.ts
+++ b/src/agents/embedded-agent-runner/run/failover-policy.ts
@@ -50,6 +50,7 @@ type PromptDecisionParams = {
   failoverFailure: boolean;
   failoverReason: FailoverReason | null;
   harnessOwnsTransport?: boolean;
+  promptTimeoutFallbackSafe?: boolean;
   profileRotated: boolean;
 };
 
@@ -179,6 +180,14 @@ export function resolveRunFailoverDecision(params: RunFailoverDecisionParams): R
       };
     }
     if (params.harnessOwnsTransport && params.failoverReason === "timeout") {
+      // Plugin harness lifecycle timeouts must stay inside the harness boundary;
+      // only prompt request timeouts proven replay-safe may enter model fallback.
+      if (params.promptTimeoutFallbackSafe === true && params.fallbackConfigured) {
+        return {
+          action: "fallback_model",
+          reason: "timeout",
+        };
+      }
       return {
         action: "surface_error",
         reason: params.failoverReason,