diff --git a/doc/plugins/PLUGIN_SPEC.md b/doc/plugins/PLUGIN_SPEC.md
index 715a0476d5a..e6d96c59d44 100644
--- a/doc/plugins/PLUGIN_SPEC.md
+++ b/doc/plugins/PLUGIN_SPEC.md
@@ -538,7 +538,9 @@ expected current status, so a disable or uninstall during a retry wins. Server
 shutdown cancels pending retries and waits for running ones. Runs that need the plugin see a
 worker that is not running, which setup retries within its bounded budget. After
 the last retry, the plugin becomes `error` with that same prefix. A run that
-needs the plugin then re-activates it on demand, at most once a minute. Any
+needs the plugin then re-activates it on demand, at most once a minute. A run that resumes its exact sandbox lease after a
+restart waits up to 60 seconds for a re-activating sandbox provider's worker
+before it reports the worker unavailable. Any
 other activation failure, such as a bad manifest, a worker that exits during
 `initialize`, or a version mismatch, makes the plugin `error` at once. The next
 server boot retries it once.
diff --git a/server/src/__tests__/environment-runtime.test.ts b/server/src/__tests__/environment-runtime.test.ts
index 509646dc29b..57fae63cda3 100644
--- a/server/src/__tests__/environment-runtime.test.ts
+++ b/server/src/__tests__/environment-runtime.test.ts
@@ -4036,13 +4036,30 @@ describeEmbeddedPostgres("environmentRuntimeService", () => {
     const call = vi.fn();
     const requestActivationTimeoutRecovery = vi.fn(() => true);
     const workerManager = { isRunning: () => false, call, getWorker: () => undefined, requestActivationTimeoutRecovery } as unknown as PluginWorkerManager;
-    const error = await environmentRuntimeService(db, { pluginWorkerManager: workerManager })
+    const error = await environmentRuntimeService(db, { pluginWorkerManager: workerManager, pluginWorkerResumeWaitMs: 50, pluginWorkerReadyPollMs: 5 })
       .resumeRunLease({ environment: seeded.environment, lease }).catch(caught => caught);
     expect(error).toBeInstanceOf(PluginWorkerUnavailableError);
     expect(call).not.toHaveBeenCalled();
     expect(requestActivationTimeoutRecovery).toHaveBeenCalledTimes(status === "error" ? 1 : 0);
   });
 
+  it("resumes the exact lease once a re-activating plugin's worker comes back within the wait", async () => {
+    const seeded = await seedReusablePluginSandboxLease("paperclip_runner");
+    await environmentService(db).releaseLease(seeded.reusableLease.id, "released", { cleanupStatus: "success" });
+    const lease = (await environmentService(db).getLeaseById(seeded.reusableLease.id))!;
+    let checks = 0;
+    const call = vi.fn(async (_id: string, method: string) => {
+      if (method !== "environmentResumeLease") throw new Error("Only exact resume is permitted");
+      return { providerLeaseId: lease.providerLeaseId, metadata: { remoteCwd: "/workspace" } };
+    });
+    const workerManager = { isRunning: () => ++checks > 3, call,
+      getWorker: () => ({ supportedMethods: ["environmentResumeLease", "environmentReleaseLease", "environmentDestroyLease"] }),
+    } as unknown as PluginWorkerManager;
+    await expect(environmentRuntimeService(db, { pluginWorkerManager: workerManager, pluginWorkerResumeWaitMs: 5_000, pluginWorkerReadyPollMs: 5 })
+      .resumeRunLease({ environment: seeded.environment, lease })).resolves.toMatchObject({ providerLeaseId: lease.providerLeaseId });
+    expect(call).toHaveBeenCalledOnce();
+  });
+
   it.each([
     { timeoutMs: 300_000, rpcTimeoutMs: 330_000 },
     { timeoutMs: 1234, rpcTimeoutMs: 31_234 },
diff --git a/server/src/services/environment-runtime.ts b/server/src/services/environment-runtime.ts
index a567bcffcc8..62294857264 100644
--- a/server/src/services/environment-runtime.ts
+++ b/server/src/services/environment-runtime.ts
@@ -782,6 +782,7 @@ export type ProviderResourceDisposition =
   | "destroy";
 
 const DEFAULT_PLUGIN_SANDBOX_WORKER_READY_TIMEOUT_MS = 5_000;
+const DEFAULT_PLUGIN_SANDBOX_WORKER_RESUME_WAIT_MS = 60_000;
 const DEFAULT_PLUGIN_SANDBOX_WORKER_READY_POLL_MS = 100;
 
 const DEFAULT_DEFERRED_ORPHAN_CLEANUP_BUFFER_LIMIT = 256;
@@ -1338,6 +1339,7 @@ function createSandboxEnvironmentDriver(
     readOnlyInspection?: boolean;
     pluginWorkerReadyTimeoutMs?: number;
     pluginWorkerReadyPollMs?: number;
+    pluginWorkerResumeWaitMs?: number;
     deferredOrphanCleanupBufferLimit?: number;
     orphanCleanupSpool?: SandboxOrphanCleanupSpool;
     orphanCleanupSpoolDir?: string;
@@ -1346,6 +1348,7 @@ function createSandboxEnvironmentDriver(
   const pluginWorkerManager = options.pluginWorkerManager;
   const pluginWorkerReadyTimeoutMs = options.pluginWorkerReadyTimeoutMs ?? DEFAULT_PLUGIN_SANDBOX_WORKER_READY_TIMEOUT_MS;
   const pluginWorkerReadyPollMs = options.pluginWorkerReadyPollMs ?? DEFAULT_PLUGIN_SANDBOX_WORKER_READY_POLL_MS;
+  const pluginWorkerResumeWaitMs = options.pluginWorkerResumeWaitMs ?? DEFAULT_PLUGIN_SANDBOX_WORKER_RESUME_WAIT_MS;
   // The buffer holds at least one orphan, so a zero or negative override never
   // drops every buffered record.
   const deferredOrphanCleanupBufferLimit = Math.max(
@@ -2702,7 +2705,9 @@ function createSandboxEnvironmentDriver(
         && !pluginWorkerManager.isRunning(pluginId)) {
         const plugin = await resolvePluginSandboxProviderDriverById({ db, pluginId, driverKey: providerKey });
         if (plugin && (plugin.plugin.status === "ready" || pluginWorkerManager.requestActivationTimeoutRecovery?.(plugin.plugin))) {
-          throw new PluginWorkerUnavailableError({ pluginId, workerStatus: pluginWorkerManager.getWorker(pluginId)?.status ?? null,
+          const deadline = Date.now() + Math.max(0, pluginWorkerResumeWaitMs);
+          while (!pluginWorkerManager.isRunning(pluginId) && Date.now() < deadline) await delay(Math.max(1, pluginWorkerReadyPollMs));
+          if (!pluginWorkerManager.isRunning(pluginId)) throw new PluginWorkerUnavailableError({ pluginId, workerStatus: pluginWorkerManager.getWorker(pluginId)?.status ?? null,
             message: `Sandbox provider "${providerKey}" is installed via plugin "${plugin.plugin.pluginKey}", but its worker is not running.` });
         }
       }
@@ -3786,6 +3791,7 @@ export function environmentRuntimeService(
     readOnlyInspection?: boolean;
     pluginWorkerReadyTimeoutMs?: number;
     pluginWorkerReadyPollMs?: number;
+    pluginWorkerResumeWaitMs?: number;
     deferredOrphanCleanupBufferLimit?: number;
     orphanCleanupSpool?: SandboxOrphanCleanupSpool;
     orphanCleanupSpoolDir?: string;
@@ -3803,6 +3809,7 @@ export function environmentRuntimeService(
       readOnlyInspection: options.readOnlyInspection,
       pluginWorkerReadyTimeoutMs: options.pluginWorkerReadyTimeoutMs,
       pluginWorkerReadyPollMs: options.pluginWorkerReadyPollMs,
+      pluginWorkerResumeWaitMs: options.pluginWorkerResumeWaitMs,
       deferredOrphanCleanupBufferLimit: options.deferredOrphanCleanupBufferLimit,
       orphanCleanupSpool: options.orphanCleanupSpool,
       orphanCleanupSpoolDir: options.orphanCleanupSpoolDir,