diff --git a/apps/worker/src/automation-sandbox.test.ts b/apps/worker/src/automation-sandbox.test.ts
index 80c7195b..bfc237d7 100644
--- a/apps/worker/src/automation-sandbox.test.ts
+++ b/apps/worker/src/automation-sandbox.test.ts
@@ -558,7 +558,9 @@ describe("fresh automation sandbox", () => {
 
     await runInFreshAutomationSandbox({ ...input, keepPaused: true, resumeState: { sandboxId: "sandbox-1" } }, dependencies);
 
-    expect(client.resume).toHaveBeenCalledWith({ sandboxId: "sandbox-1" });
+    // The saved state leaves out the API key; the resumed session's file
+    // transfers need it.
+    expect(client.resume).toHaveBeenCalledWith({ apiKey: "daytona-test", sandboxId: "sandbox-1" });
     expect(dependencies.createSession).not.toHaveBeenCalled();
     expect(dependencies.configure).not.toHaveBeenCalled();
     expect(dependencies.prepare).not.toHaveBeenCalled();
diff --git a/apps/worker/src/automation-sandbox.ts b/apps/worker/src/automation-sandbox.ts
index bb041080..df72dd53 100644
--- a/apps/worker/src/automation-sandbox.ts
+++ b/apps/worker/src/automation-sandbox.ts
@@ -19,6 +19,7 @@ import {
   maxDaytonaSandboxBaseNameLength,
   prepareDaytonaSandbox,
   replaceDaytonaSandboxSecrets,
+  resumeDaytonaSandbox,
   sandboxesLeftAfterFailedCreation,
   type DaytonaSandboxSecretMount,
 } from "./sandbox.js";
@@ -265,7 +266,7 @@ export async function runInFreshAutomationSandbox<T>(
     if (input.resumeState) {
       try {
         session = await abortable(
-          client.resume(await client.deserializeSessionState(input.resumeState)),
+          resumeDaytonaSandbox(client, input.resumeState, input.config),
           input.signal,
         );
         // Daytona recreates a sandbox it no longer has; that one needs setup.
diff --git a/apps/worker/src/investigate.ts b/apps/worker/src/investigate.ts
index 8e372308..fde06172 100644
--- a/apps/worker/src/investigate.ts
+++ b/apps/worker/src/investigate.ts
@@ -90,6 +90,7 @@ import {
   createDaytonaSandboxSession,
   prepareDaytonaSandbox,
   pauseDaytonaSandbox,
+  resumeDaytonaSandbox,
 } from "./sandbox.js";
 import { startSandboxMeter, type SandboxMeter } from "./sandbox-metering.js";
 import { agentUsageIsBillable, recordAgentRunUsage } from "./agent-usage.js";
@@ -967,9 +968,7 @@ export async function runInvestigationAgent(
     const persistedState = sessionRuntime?.sandboxSessionState;
     if (threadMode && persistedState) {
       try {
-        session = await client.resume(
-          await client.deserializeSessionState(persistedState),
-        );
+        session = await resumeDaytonaSandbox(client, persistedState, config);
       } catch (error) {
         // Daytona deletes a paused thread sandbox after a day; the thread
         // continues in a fresh one.
diff --git a/apps/worker/src/sandbox.test.ts b/apps/worker/src/sandbox.test.ts
index 97e7ebf2..c081f3d7 100644
--- a/apps/worker/src/sandbox.test.ts
+++ b/apps/worker/src/sandbox.test.ts
@@ -1,4 +1,7 @@
-import type { DaytonaSandboxSession } from "@openai/agents-extensions/sandbox/daytona";
+import type {
+  DaytonaSandboxClient,
+  DaytonaSandboxSession,
+} from "@openai/agents-extensions/sandbox/daytona";
 import { describe, expect, it, vi } from "vitest";
 import {
   closeDaytonaSandbox,
@@ -10,6 +13,7 @@ import {
   prepareDaytonaPatchSandbox,
   prepareDaytonaSandbox,
   replaceDaytonaSandboxSecrets,
+  resumeDaytonaSandbox,
   sandboxDeletedAfterFailedCreation,
   sandboxesLeftAfterFailedCreation,
 } from "./sandbox.js";
@@ -776,6 +780,31 @@ describe("Daytona sandbox cleanup", () => {
   });
 });
 
+describe("Daytona sandbox resume", () => {
+  it("gives the resumed session the API key its saved state left out", async () => {
+    const session = { state: { sandboxId: "sandbox-1" } };
+    const client = {
+      deserializeSessionState: vi.fn(async (state: Record<string, unknown>) => ({
+        ...state,
+        apiKey: undefined,
+      })),
+      resume: vi.fn().mockResolvedValue(session),
+    };
+
+    await expect(
+      resumeDaytonaSandbox(
+        client as unknown as DaytonaSandboxClient,
+        { sandboxId: "sandbox-1" },
+        { daytonaApiKey: "daytona-key" },
+      ),
+    ).resolves.toBe(session);
+    expect(client.resume).toHaveBeenCalledWith({
+      apiKey: "daytona-key",
+      sandboxId: "sandbox-1",
+    });
+  });
+});
+
 describe("Daytona thread sandbox pause", () => {
   it("stops the sandbox through the session", async () => {
     const harness = cleanupHarness();
diff --git a/apps/worker/src/sandbox.ts b/apps/worker/src/sandbox.ts
index 3c436ec4..6beb68f1 100644
--- a/apps/worker/src/sandbox.ts
+++ b/apps/worker/src/sandbox.ts
@@ -497,6 +497,17 @@ export async function replaceDaytonaSandboxSecrets(
   }
 }
 
+// A paused sandbox's saved state leaves out the API key. The resumed
+// session gets it back, because its file transfers read it from the state.
+export async function resumeDaytonaSandbox(
+  client: DaytonaSandboxClient,
+  persistedState: Record<string, unknown>,
+  config: DaytonaClientConfig,
+): Promise<DaytonaSandboxSession> {
+  const state = await client.deserializeSessionState(persistedState);
+  return client.resume({ ...state, apiKey: config.daytonaApiKey });
+}
+
 // A thread sandbox that fails to stop keeps running until Daytona's
 // auto-stop, and the next turn resumes or replaces it. The failure is
 // reported without failing the turn that already has its answer.