diff --git a/apps/desktop/src/main/services/chat/agentChatService.test.ts b/apps/desktop/src/main/services/chat/agentChatService.test.ts
index ef5e416cc..9b45bf1b2 100644
--- a/apps/desktop/src/main/services/chat/agentChatService.test.ts
+++ b/apps/desktop/src/main/services/chat/agentChatService.test.ts
@@ -2822,6 +2822,63 @@ describe("createAgentChatService", () => {
       }
     });
 
+    it("repoints orchestration bundle path when lane placement changes", async () => {
+      const { orchestrationService, created } = await createLoadedOrchestrationRun("S-lead-placement");
+      const movedWorktree = path.join(tmpRoot, "lane-vm-mirror");
+      fs.mkdirSync(movedWorktree, { recursive: true });
+      try {
+        const { service, laneService } = createService({
+          getOrchestrationService: () => orchestrationService,
+        });
+        const session = await service.createSession({
+          laneId: "lane-1",
+          provider: "claude",
+          model: "sonnet",
+          modelId: "anthropic/claude-sonnet-4-6",
+          interactionMode: "orchestrator-lead",
+          orchestrationRunId: created.runId,
+          orchestrationRole: "lead",
+          orchestrationBundlePath: created.manifest.bundlePath,
+        });
+
+        const lanes = await laneService.list();
+        const lane1 = lanes.find((entry: { id: string }) => entry.id === "lane-1");
+        expect(lane1).toBeTruthy();
+        lane1.worktreePath = movedWorktree;
+        vi.mocked(laneService.getLaneBaseAndBranch).mockImplementation((laneId: string) => {
+          const lane = lanes.find((entry: { id: string }) => entry.id === laneId);
+          if (!lane) {
+            return {
+              baseRef: "main",
+              branchRef: "feature/selected",
+              worktreePath: tmpRoot,
+              laneType: "feature",
+              runtimePlacement: "local",
+            };
+          }
+          return {
+            baseRef: "main",
+            branchRef: lane.branchRef,
+            worktreePath: lane.worktreePath,
+            laneType: lane.laneType,
+            runtimePlacement: "local",
+          };
+        });
+
+        service.handleLanePlacementChanged({
+          laneId: "lane-1",
+          from: "macos-vm",
+          to: "local",
+        });
+
+        const expectedBundlePath = path.join(movedWorktree, ".ade", "orchestration", created.runId);
+        expect(readPersistedChatState(session.id).orchestrationBundlePath).toBe(expectedBundlePath);
+        expect(orchestrationService.getBundlePathForRun(created.runId)).toBe(expectedBundlePath);
+      } finally {
+        await orchestrationService.dispose();
+      }
+    });
+
     it("attaches ADE orchestration tools to OpenCode orchestrator sessions through MCP", async () => {
       vi.mocked(streamText).mockReturnValue({
         fullStream: (async function* () {
diff --git a/apps/desktop/src/main/services/chat/agentChatService.ts b/apps/desktop/src/main/services/chat/agentChatService.ts
index 4b522b061..1f99f1cf4 100644
--- a/apps/desktop/src/main/services/chat/agentChatService.ts
+++ b/apps/desktop/src/main/services/chat/agentChatService.ts
@@ -23351,6 +23351,17 @@ export function createAgentChatService(args: {
           error: error instanceof Error ? error.message : String(error),
         });
       }
+      const runId = managed.session.orchestrationRunId?.trim();
+      const worktree = managed.laneWorktreePath?.trim();
+      if (runId && worktree) {
+        const nextBundlePath = path.join(worktree, ".ade", "orchestration", runId);
+        const currentBundlePath = managed.session.orchestrationBundlePath?.trim();
+        if (currentBundlePath !== nextBundlePath) {
+          managed.session.orchestrationBundlePath = nextBundlePath;
+          persistChatState(managed);
+          getOrchestrationService?.()?.relocateRunBundle(runId, nextBundlePath);
+        }
+      }
       const message = event.to === "local"
         ? "Lane detached from Mac VM; further turns run locally."
         : "Lane attached to Mac VM; further turns run inside the VM at /Volumes/My Shared Files.";
diff --git a/apps/desktop/src/main/services/orchestration/orchestrationService.test.ts b/apps/desktop/src/main/services/orchestration/orchestrationService.test.ts
index 438db49ac..8fe445aaf 100644
--- a/apps/desktop/src/main/services/orchestration/orchestrationService.test.ts
+++ b/apps/desktop/src/main/services/orchestration/orchestrationService.test.ts
@@ -209,6 +209,24 @@ describe("orchestrationService", () => {
     await restarted.dispose();
   });
 
+  it("relocates in-memory runtime when the lane worktree bundle path changes", async () => {
+    const svc = createOrchestrationService({ resolveLaneWorktree: () => lane });
+    const movedWorktree = path.join(lane, "vm-mirror-worktree");
+    await fsp.mkdir(movedWorktree, { recursive: true });
+    const { runId, manifest } = await svc.runCreate({
+      laneId: "L-1",
+      leadSessionId: "S-lead",
+      bundleRoot: lane,
+      title: "Placement move",
+    });
+    const movedBundlePath = path.join(movedWorktree, ".ade", "orchestration", runId);
+    expect(svc.getBundlePathForRun(runId)).toBe(manifest.bundlePath);
+
+    svc.relocateRunBundle(runId, movedBundlePath);
+    expect(svc.getBundlePathForRun(runId)).toBe(movedBundlePath);
+    await svc.dispose();
+  });
+
   it("skips stale discovery index entries whose manifest is gone", async () => {
     const svc = createOrchestrationService({ resolveLaneWorktree: () => lane });
     const stale = await svc.runCreate({
diff --git a/apps/desktop/src/main/services/orchestration/orchestrationService.ts b/apps/desktop/src/main/services/orchestration/orchestrationService.ts
index fcc885085..5f3f8b1ec 100644
--- a/apps/desktop/src/main/services/orchestration/orchestrationService.ts
+++ b/apps/desktop/src/main/services/orchestration/orchestrationService.ts
@@ -407,6 +407,22 @@ export function createOrchestrationService(deps: OrchestrationServiceDeps) {
       .join(",");
   }
 
+  function relocateRuntimeBundlePath(runtime: RunRuntime, bundlePath: string): void {
+    if (runtime.bundlePath === bundlePath) return;
+    if (runtime.watcher) {
+      void runtime.watcher.close().catch(() => undefined);
+      runtime.watcher = null;
+    }
+    if (runtime.watcherDebounceTimer) {
+      clearTimeout(runtime.watcherDebounceTimer);
+      runtime.watcherDebounceTimer = null;
+    }
+    runtime.bundlePath = bundlePath;
+    runtime.manifest = null;
+    runtime.planMd = null;
+    runtime.suspended = false;
+  }
+
   function getOrCreateRuntime(
     runId: string,
     bundlePath: string,
@@ -427,7 +443,9 @@ export function createOrchestrationService(deps: OrchestrationServiceDeps) {
         suspended: false,
       };
       runs.set(runId, runtime);
+      return runtime;
     }
+    relocateRuntimeBundlePath(runtime, bundlePath);
     return runtime;
   }
 
@@ -1442,8 +1460,13 @@ export function createOrchestrationService(deps: OrchestrationServiceDeps) {
     });
   }
 
+  function relocateRunBundle(runId: string, bundlePath: string): void {
+    getOrCreateRuntime(runId, bundlePath);
+  }
+
   return {
     runCreate,
+    relocateRunBundle,
     bundleRead,
     manifestReadSection,
     manifestPatch,