diff --git a/src/main/runtime/file-watcher-host.test.ts b/src/main/runtime/file-watcher-host.test.ts
index 4aef254312f..77f6e3efa06 100644
--- a/src/main/runtime/file-watcher-host.test.ts
+++ b/src/main/runtime/file-watcher-host.test.ts
@@ -134,12 +134,12 @@ describe('watchFileExplorerInWorker', () => {
     worker.emit('message', { type: 'ready' })
     const dispose = await promise
 
-    dispose()
+    await dispose()
     expect(worker.postedMessages).toContainEqual({ type: 'unsubscribe' })
     expect(worker.terminated).toBe(true)
 
     // Idempotent: a second dispose does nothing further.
-    dispose()
+    await dispose()
     expect(
       worker.postedMessages.filter((m) => (m as { type?: string }).type === 'unsubscribe')
     ).toHaveLength(1)
@@ -151,7 +151,7 @@ describe('watchFileExplorerInWorker', () => {
     const worker = lastWorker()
     worker.emit('message', { type: 'ready' })
     const dispose = await promise
-    dispose()
+    await dispose()
     onEvents.mockClear()
 
     worker.emit('message', {
diff --git a/src/main/runtime/file-watcher-host.ts b/src/main/runtime/file-watcher-host.ts
index 55da4aa7728..90bd9ec8598 100644
--- a/src/main/runtime/file-watcher-host.ts
+++ b/src/main/runtime/file-watcher-host.ts
@@ -36,7 +36,7 @@ function getFileWatcherWorkerPath(): string {
 export function watchFileExplorerInWorker(
   rootPath: string,
   callback: (events: FsChangeEvent[]) => void
-): Promise<() => void> {
+): Promise<() => Promise<void>> {
   return new Promise((resolve, reject) => {
     const worker = new Worker(getFileWatcherWorkerPath(), {
       workerData: { rootPath, ignore: RUNTIME_FILE_WATCH_IGNORE }
@@ -45,7 +45,10 @@ export function watchFileExplorerInWorker(
     let ready = false
     let disposed = false
 
-    const dispose = (): void => {
+    // Why: returns a promise that resolves once the worker is actually down, so
+    // the shutdown drain (awaitRuntimeFileWatcherUnsubscribes) doesn't finish
+    // while the native watcher thread is still alive.
+    const dispose = async (): Promise<void> => {
       if (disposed) {
         return
       }
@@ -57,7 +60,10 @@ export function watchFileExplorerInWorker(
       } catch {
         // Worker already gone — terminate below covers it.
       }
-      void worker.terminate()
+      await worker.terminate().then(
+        () => undefined,
+        () => undefined
+      )
     }
 
     worker.on('message', (message: FileWatcherWorkerMessage) => {
diff --git a/src/main/runtime/file-watcher-worker.ts b/src/main/runtime/file-watcher-worker.ts
index 2dd05d655ae..3325b43c377 100644
--- a/src/main/runtime/file-watcher-worker.ts
+++ b/src/main/runtime/file-watcher-worker.ts
@@ -36,6 +36,20 @@ if (!parentPort) {
 
 const port = parentPort
 
+/** Report a watcher failure to the host and ask the renderer to refresh from
+ *  scratch (the overflow event), so a mid-stream error never leaves the
+ *  explorer silently stale. */
+function reportWatchError(err: unknown): void {
+  port.postMessage({
+    type: 'error',
+    message: err instanceof Error ? err.message : String(err)
+  } satisfies FileWatcherWorkerMessage)
+  port.postMessage({
+    type: 'events',
+    events: [{ kind: 'overflow', absolutePath: data.rootPath }]
+  } satisfies FileWatcherWorkerMessage)
+}
+
 /** Run an async mapper over items with a bounded number in flight at once, so a
  *  large batch can't occupy every libuv threadpool thread in this worker. */
 async function mapWithConcurrency<T, R>(
@@ -71,15 +85,7 @@ async function main(): Promise<void> {
     data.rootPath,
     (err, events) => {
       if (err) {
-        // Surface the error and ask the renderer to refresh from scratch.
-        port.postMessage({
-          type: 'error',
-          message: err.message
-        } satisfies FileWatcherWorkerMessage)
-        port.postMessage({
-          type: 'events',
-          events: [{ kind: 'overflow', absolutePath: data.rootPath }]
-        } satisfies FileWatcherWorkerMessage)
+        reportWatchError(err)
         return
       }
       // Why: large watcher batches usually mean a generated directory or branch
@@ -103,9 +109,13 @@ async function main(): Promise<void> {
           }
           return { kind: event.type, absolutePath: event.path, isDirectory }
         }
-      ).then((mapped) => {
-        port.postMessage({ type: 'events', events: mapped } satisfies FileWatcherWorkerMessage)
-      })
+      )
+        .then((mapped) => {
+          port.postMessage({ type: 'events', events: mapped } satisfies FileWatcherWorkerMessage)
+        })
+        // Why: without this, a throwing postMessage / stat becomes an unhandled
+        // rejection that crashes the worker silently. Surface it instead.
+        .catch((err: unknown) => reportWatchError(err))
     },
     { ignore: data.ignore }
   )
diff --git a/src/main/runtime/orca-runtime-files.ts b/src/main/runtime/orca-runtime-files.ts
index e3e08a01552..62deef6b63c 100644
--- a/src/main/runtime/orca-runtime-files.ts
+++ b/src/main/runtime/orca-runtime-files.ts
@@ -298,7 +298,7 @@ export class RuntimeFileCommands {
     // recursive crawl can't starve the main/`serve` process (issue #5308).
     const dispose = await watchFileExplorerInWorker(rootPath, callback)
     return () => {
-      trackRuntimeFileWatcherUnsubscribe(rootPath, async () => dispose())
+      trackRuntimeFileWatcherUnsubscribe(rootPath, dispose)
     }
   }