diff --git a/packages/ocap-kernel/CHANGELOG.md b/packages/ocap-kernel/CHANGELOG.md
index e2903d804..6b7583524 100644
--- a/packages/ocap-kernel/CHANGELOG.md
+++ b/packages/ocap-kernel/CHANGELOG.md
@@ -44,6 +44,9 @@ and this project adheres to [Semantic Versioning](https://semver.org/spec/v2.0.0
 - Use length-prefixed framing for remote messages so payloads larger than the underlying transport's per-frame cutoff (e.g. `@libp2p/webrtc`'s 16 KB datachannel limit) are reassembled correctly on the receiver ([#957](https://github.com/MetaMask/ocap-kernel/pull/957))
   - Replace `byteStream` with `lpStream` on every remote channel; the byte-oriented stream did not preserve `write()` boundaries, so any message the transport split into multiple frames was parsed from the first frame only, silently dropped without acknowledgement, and the sender retried until giving up after `MAX_RETRIES`
   - Surface receiver-side framing-cap violations (`InvalidDataLengthError`, `InvalidDataLengthLengthError`) as `ResourceLimitError` with `limitType: 'messageSize'` so size errors look the same whether they tripped on the sender's `validateMessageSize` or the receiver's framing decoder
+- Restore IO channels for persisted subclusters at kernel init so re-incarnated vats find their IOService references live ([#963](https://github.com/MetaMask/ocap-kernel/pull/963))
+  - `SubclusterManager.restorePersistedIOChannels()` walks every persisted subcluster, finds those whose config declares `io`, and re-creates the channels via `IOManager` before `initializeAllVats` runs
+  - Without this, any vat that opened an IO channel via `launchSubcluster` lost its channel across `daemon stop` / `daemon start` and silently held a dead IOService reference
 
 ## [0.7.0]
 
diff --git a/packages/ocap-kernel/src/Kernel.ts b/packages/ocap-kernel/src/Kernel.ts
index ec4956661..6cff64962 100644
--- a/packages/ocap-kernel/src/Kernel.ts
+++ b/packages/ocap-kernel/src/Kernel.ts
@@ -282,6 +282,12 @@ export class Kernel {
     // longer have a config, to ensure that orphaned vats aren't started
     this.#subclusterManager.initSystemSubclusters(configs);
 
+    // Re-create IO channels for persisted subclusters whose configs
+    // declare them. This must happen before `initializeAllVats` so
+    // that re-incarnated vats find their IOService references live
+    // when they make their first method call.
+    await this.#subclusterManager.restorePersistedIOChannels();
+
     // Start all vats that were previously running before starting the queue
     // This ensures that any messages in the queue have their target vats ready
     await this.#vatManager.initializeAllVats();
diff --git a/packages/ocap-kernel/src/vats/SubclusterManager.test.ts b/packages/ocap-kernel/src/vats/SubclusterManager.test.ts
index afaa9c15e..165da7fb3 100644
--- a/packages/ocap-kernel/src/vats/SubclusterManager.test.ts
+++ b/packages/ocap-kernel/src/vats/SubclusterManager.test.ts
@@ -821,4 +821,119 @@ describe('SubclusterManager', () => {
       ).not.toHaveBeenCalled();
     });
   });
+
+  describe('restorePersistedIOChannels', () => {
+    const makeMockIOManager = () => ({
+      createChannels: vi.fn().mockResolvedValue(undefined),
+      destroyChannels: vi.fn().mockResolvedValue(undefined),
+    });
+
+    const subclusterWithIO = (
+      id: string,
+      io: Record<string, { type: 'socket'; path: string }>,
+    ): Subcluster => ({
+      id,
+      config: {
+        bootstrap: 'svc',
+        vats: { svc: { sourceSpec: 'svc.js' } },
+        io,
+      },
+      vats: { svc: 'v1' as VatId },
+    });
+
+    const subclusterWithoutIO = (id: string): Subcluster => ({
+      id,
+      config: createMockClusterConfig(`s-${id}`),
+      vats: { [`s-${id}Vat`]: 'v1' as VatId },
+    });
+
+    it('re-creates channels for every persisted subcluster declaring io', async () => {
+      const ioA = { llm: { type: 'socket' as const, path: '/tmp/a.sock' } };
+      const ioB = { wire: { type: 'socket' as const, path: '/tmp/b.sock' } };
+      mockKernelStore.getSubclusters.mockReturnValue([
+        subclusterWithIO('s1', ioA),
+        subclusterWithIO('s2', ioB),
+      ]);
+      const ioManager = makeMockIOManager();
+      const mgr = new SubclusterManager({
+        kernelStore: mockKernelStore,
+        kernelQueue: mockKernelQueue,
+        vatManager: mockVatManager,
+        getKernelService: mockGetKernelService,
+        queueMessage: mockQueueMessage,
+        ioManager: ioManager as never,
+      });
+
+      await mgr.restorePersistedIOChannels();
+
+      expect(ioManager.createChannels).toHaveBeenCalledTimes(2);
+      expect(ioManager.createChannels).toHaveBeenCalledWith('s1', ioA);
+      expect(ioManager.createChannels).toHaveBeenCalledWith('s2', ioB);
+    });
+
+    it('skips subclusters whose config does not declare io', async () => {
+      mockKernelStore.getSubclusters.mockReturnValue([
+        subclusterWithoutIO('s1'),
+        subclusterWithIO('s2', {
+          io: { type: 'socket' as const, path: '/tmp/s2.sock' },
+        }),
+      ]);
+      const ioManager = makeMockIOManager();
+      const mgr = new SubclusterManager({
+        kernelStore: mockKernelStore,
+        kernelQueue: mockKernelQueue,
+        vatManager: mockVatManager,
+        getKernelService: mockGetKernelService,
+        queueMessage: mockQueueMessage,
+        ioManager: ioManager as never,
+      });
+
+      await mgr.restorePersistedIOChannels();
+
+      expect(ioManager.createChannels).toHaveBeenCalledTimes(1);
+      expect(ioManager.createChannels).toHaveBeenCalledWith(
+        's2',
+        expect.objectContaining({ io: expect.anything() }),
+      );
+    });
+
+    it('is a no-op when no IOManager was provided', async () => {
+      mockKernelStore.getSubclusters.mockReturnValue([
+        subclusterWithIO('s1', {
+          llm: { type: 'socket' as const, path: '/tmp/a.sock' },
+        }),
+      ]);
+      // Default subclusterManager from beforeEach has no ioManager;
+      // a missing manager must not cause an error here.
+      expect(
+        await subclusterManager.restorePersistedIOChannels(),
+      ).toBeUndefined();
+    });
+
+    it('continues past a per-subcluster failure', async () => {
+      mockKernelStore.getSubclusters.mockReturnValue([
+        subclusterWithIO('s1', {
+          llm: { type: 'socket' as const, path: '/tmp/a.sock' },
+        }),
+        subclusterWithIO('s2', {
+          wire: { type: 'socket' as const, path: '/tmp/b.sock' },
+        }),
+      ]);
+      const ioManager = makeMockIOManager();
+      ioManager.createChannels.mockImplementationOnce(async () => {
+        throw new Error('socket in use');
+      });
+      const mgr = new SubclusterManager({
+        kernelStore: mockKernelStore,
+        kernelQueue: mockKernelQueue,
+        vatManager: mockVatManager,
+        getKernelService: mockGetKernelService,
+        queueMessage: mockQueueMessage,
+        ioManager: ioManager as never,
+      });
+
+      expect(await mgr.restorePersistedIOChannels()).toBeUndefined();
+      expect(ioManager.createChannels).toHaveBeenCalledTimes(2);
+    });
+  });
 });
diff --git a/packages/ocap-kernel/src/vats/SubclusterManager.ts b/packages/ocap-kernel/src/vats/SubclusterManager.ts
index cc0a9c74a..a32ac7a5d 100644
--- a/packages/ocap-kernel/src/vats/SubclusterManager.ts
+++ b/packages/ocap-kernel/src/vats/SubclusterManager.ts
@@ -368,6 +368,56 @@ export class SubclusterManager {
     this.#restorePersistedSystemSubclusters(configs);
   }
 
+  /**
+   * Re-create IO channels for every persisted subcluster whose config
+   * declares one.
+   *
+   * IO channels (`config.io`) are external to the kernel's durable
+   * state — they're live OS-process resources (Unix sockets, pipes,
+   * etc.) backed by the host's IOManager. `launchSubcluster` creates
+   * them at subcluster-launch time, but on a kernel restart the vats
+   * get re-incarnated from persisted state without going through
+   * `launchSubcluster` again, so any IO channels they were using are
+   * gone. This method bridges that gap: invoked from the kernel's
+   * init path before `initializeAllVats`, it walks the persisted
+   * subcluster table and re-creates each subcluster's declared IO
+   * channels so the re-incarnated vats find their IOService
+   * references live and ready when they make their first method call.
+   *
+   * If a particular subcluster's `createChannels` call fails (e.g.
+   * the socket path is now in use by another process), the failure
+   * is logged but does not abort the broader init — other
+   * subclusters can still come up. Vats backed by the failed
+   * subcluster will see method calls on their IOServices fail at
+   * first use.
+   *
+   * No-op when no IOManager was provided to this SubclusterManager.
+   */
+  async restorePersistedIOChannels(): Promise<void> {
+    if (!this.#ioManager) {
+      return;
+    }
+    for (const subcluster of this.#kernelStore.getSubclusters()) {
+      if (!subcluster.config.io) {
+        continue;
+      }
+      try {
+        await this.#ioManager.createChannels(
+          subcluster.id,
+          subcluster.config.io,
+        );
+        this.#logger.info(
+          `Restored IO channels for persisted subcluster ${subcluster.id}`,
+        );
+      } catch (error) {
+        this.#logger.error(
+          `Failed to restore IO channels for subcluster ${subcluster.id}:`,
+          error,
+        );
+      }
+    }
+  }
+
   /**
    * Launch new system subclusters that aren't already in persistence.
    * This must be called after the kernel queue is running since launchSubcluster