diff --git a/src/main/runtime/files/watch/file-watches.ts b/src/main/runtime/files/watch/file-watches.ts
index 5b06f0ffcc1..6fb4a0d5431 100644
--- a/src/main/runtime/files/watch/file-watches.ts
+++ b/src/main/runtime/files/watch/file-watches.ts
@@ -14,7 +14,7 @@ import type { DirEntry, FsChangeEvent } from '../../../../shared/filesystem-entr
 import { sortDirEntries } from '../../../../shared/file-name-sort'
 import { resolveAuthorizedPath } from '../../../ipc/filesystem/filesystem-auth'
 import { resolveRuntimeAuthorizedPath } from '../chat-scratch-file-root'
-import { watchWindowsRuntimeFileExplorer } from './windows-file-watch'
+import { WindowsRuntimeWatchPool } from './windows-runtime-watch-pool'
 import { beginWatcherInstall } from '../../../ipc/watcher-removal-gate'
 import {
   closeFileExplorerWatcherInWatcherProcess,
@@ -27,6 +27,8 @@ type RuntimeFileWatchHost = Pick<
 >
 
 export class RuntimeFileWatches {
+  private readonly windowsWatches = new WindowsRuntimeWatchPool()
+
   constructor(private readonly host: RuntimeFileWatchHost) {}
 
   async readFileExplorerDir(
@@ -63,7 +65,7 @@ export class RuntimeFileWatches {
           throw new Error('not_a_directory')
         }
         if (process.platform === 'win32') {
-          const close = watchWindowsRuntimeFileExplorer(rootPath, callback, onTerminalError)
+          const close = await this.windowsWatches.watch(rootPath, callback, onTerminalError, signal)
           return { unsubscribe: close, rootPaths: [target.path, rootPath] }
         }
         // #5308/#8212: isolate native faults and blocking crawls from main/serve.
diff --git a/src/main/runtime/files/watch/windows-runtime-watch-pool.test.ts b/src/main/runtime/files/watch/windows-runtime-watch-pool.test.ts
new file mode 100644
index 00000000000..eff782e5fa3
--- /dev/null
+++ b/src/main/runtime/files/watch/windows-runtime-watch-pool.test.ts
@@ -0,0 +1,169 @@
+import { EventEmitter } from 'node:events'
+import { afterEach, beforeEach, expect, it, vi } from 'vitest'
+import { WindowsRuntimeWatchPool } from './windows-runtime-watch-pool'
+import { WINDOWS_RUNTIME_FILE_WATCH_CLOSE_DEADLINE_MS } from './windows-file-watch'
+
+const { watchMock } = vi.hoisted(() => ({ watchMock: vi.fn() }))
+vi.mock('node:fs', () => ({ watch: watchMock }))
+
+function installWatcher(close?: () => void) {
+  const watcher = Object.assign(new EventEmitter(), {
+    close: vi.fn(() => (close ? close() : watcher.emit('close')))
+  })
+  let notify = () => undefined
+  watchMock.mockImplementationOnce((_root, _options, callback) => {
+    notify = callback
+    return watcher
+  })
+  return { watcher, notify: () => notify() }
+}
+
+beforeEach(() => {
+  vi.useFakeTimers()
+  watchMock.mockReset()
+})
+
+afterEach(() => {
+  vi.useRealTimers()
+  vi.restoreAllMocks()
+})
+
+it('shares one native watch and refresh timer across path aliases', async () => {
+  const pool = new WindowsRuntimeWatchPool()
+  const { watcher, notify } = installWatcher()
+  const callbacks = Array.from({ length: 3 }, () => vi.fn())
+  const releases = await Promise.all(
+    callbacks.map((callback, index) =>
+      pool.watch(index % 2 === 0 ? 'C:\\repo' : 'c:/REPO', callback, vi.fn())
+    )
+  )
+  expect(watchMock).toHaveBeenCalledOnce()
+  notify()
+  expect(vi.getTimerCount()).toBe(1)
+  await releases[0]()
+  expect(watcher.close).not.toHaveBeenCalled()
+  await vi.advanceTimersByTimeAsync(500)
+  expect(callbacks[0]).not.toHaveBeenCalled()
+  for (const callback of callbacks.slice(1)) {
+    expect(callback).toHaveBeenCalledExactlyOnceWith([
+      { kind: 'overflow', absolutePath: 'C:\\repo' }
+    ])
+  }
+  await Promise.all(releases.slice(1).map((release) => release()))
+  expect(watcher.close).toHaveBeenCalledOnce()
+  expect(vi.getTimerCount()).toBe(0)
+})
+
+it('keeps separate roots and runtime owners isolated', async () => {
+  const pool = new WindowsRuntimeWatchPool()
+  const anotherRuntime = new WindowsRuntimeWatchPool()
+  const first = installWatcher()
+  const second = installWatcher()
+  const third = installWatcher()
+  const releaseFirst = await pool.watch('C:\\repo', vi.fn(), vi.fn())
+  const releaseSecond = await pool.watch('C:\\other', vi.fn(), vi.fn())
+  const releaseThird = await anotherRuntime.watch('C:\\repo', vi.fn(), vi.fn())
+  expect(watchMock).toHaveBeenCalledTimes(3)
+  await releaseFirst()
+  expect(first.watcher.close).toHaveBeenCalledOnce()
+  expect(second.watcher.close).not.toHaveBeenCalled()
+  expect(third.watcher.close).not.toHaveBeenCalled()
+  await Promise.all([releaseSecond(), releaseThird()])
+})
+
+it('cancels a successor waiting on physical close without starting another watch', async () => {
+  const pool = new WindowsRuntimeWatchPool()
+  const first = installWatcher(() => undefined)
+  const release = await pool.watch('C:\\repo', vi.fn(), vi.fn())
+  const closing = release()
+  const controller = new AbortController()
+  const successor = pool.watch('C:\\repo', vi.fn(), vi.fn(), controller.signal)
+  controller.abort(new Error('successor cancelled'))
+  await expect(successor).rejects.toThrow('successor cancelled')
+  expect(watchMock).toHaveBeenCalledOnce()
+  first.watcher.emit('close')
+  await closing
+  const replacement = installWatcher()
+  const releaseReplacement = await pool.watch('C:\\repo', vi.fn(), vi.fn())
+  expect(watchMock).toHaveBeenCalledTimes(2)
+  await releaseReplacement()
+  expect(replacement.watcher.close).toHaveBeenCalledOnce()
+})
+
+it('retries failed close on the original owner before admitting a replacement', async () => {
+  vi.spyOn(console, 'error').mockImplementation(() => undefined)
+  const pool = new WindowsRuntimeWatchPool()
+  const first = installWatcher()
+  const failure = new Error('native close failed')
+  first.watcher.close.mockImplementationOnce(() => {
+    throw failure
+  })
+  const release = await pool.watch('C:\\repo', vi.fn(), vi.fn())
+  await expect(release()).rejects.toBe(failure)
+  await expect(pool.watch('C:\\repo', vi.fn(), vi.fn())).rejects.toBe(failure)
+  expect(watchMock).toHaveBeenCalledOnce()
+  await release()
+  expect(first.watcher.close).toHaveBeenCalledTimes(2)
+  installWatcher()
+  const releaseReplacement = await pool.watch('C:\\repo', vi.fn(), vi.fn())
+  expect(watchMock).toHaveBeenCalledTimes(2)
+  await releaseReplacement()
+})
+
+it('retains a timed-out root until late physical exit and keeps cleanup retryable', async () => {
+  const pool = new WindowsRuntimeWatchPool()
+  const first = installWatcher(() => undefined)
+  const release = await pool.watch('C:\\repo', vi.fn(), vi.fn())
+  const closing = release()
+  const rejected = expect(closing).rejects.toMatchObject({
+    code: 'process_unavailable',
+    physicalExit: expect.any(Promise)
+  })
+  await vi.advanceTimersByTimeAsync(WINDOWS_RUNTIME_FILE_WATCH_CLOSE_DEADLINE_MS)
+  await rejected
+  installWatcher()
+  const successor = pool.watch('C:\\repo', vi.fn(), vi.fn())
+  await Promise.resolve()
+  expect(watchMock).toHaveBeenCalledOnce()
+  const retry = release()
+  first.watcher.emit('close')
+  await retry
+  const releaseSuccessor = await successor
+  expect(watchMock).toHaveBeenCalledTimes(2)
+  expect(first.watcher.close).toHaveBeenCalledOnce()
+  await releaseSuccessor()
+})
+
+it('fans out terminal errors once and keeps old cleanup from evicting a new generation', async () => {
+  vi.spyOn(console, 'error').mockImplementation(() => undefined)
+  const pool = new WindowsRuntimeWatchPool()
+  const first = installWatcher()
+  const firstError = vi.fn()
+  const secondError = vi.fn()
+  const releaseFirst = await pool.watch('C:\\repo', vi.fn(), firstError)
+  const releaseSecond = await pool.watch('C:\\repo', vi.fn(), secondError)
+  const failure = new Error('native watcher failed')
+  first.watcher.emit('error', failure)
+  expect(firstError).toHaveBeenCalledExactlyOnceWith(failure)
+  expect(secondError).toHaveBeenCalledExactlyOnceWith(failure)
+  const replacement = installWatcher()
+  const replacementEvents = vi.fn()
+  const releaseReplacement = await pool.watch('C:\\repo', replacementEvents, vi.fn())
+  await Promise.all([releaseFirst(), releaseSecond()])
+  const releaseJoiner = await pool.watch('C:\\repo', vi.fn(), vi.fn())
+  expect(watchMock).toHaveBeenCalledTimes(2)
+  replacement.notify()
+  await vi.advanceTimersByTimeAsync(500)
+  expect(replacementEvents).toHaveBeenCalledOnce()
+  await Promise.all([releaseReplacement(), releaseJoiner()])
+})
+
+it('does not create a native watcher for an already aborted subscription', async () => {
+  const pool = new WindowsRuntimeWatchPool()
+  const controller = new AbortController()
+  controller.abort(new Error('request cancelled'))
+  await expect(pool.watch('C:\\repo', vi.fn(), vi.fn(), controller.signal)).rejects.toThrow(
+    'request cancelled'
+  )
+  expect(watchMock).not.toHaveBeenCalled()
+})
diff --git a/src/main/runtime/files/watch/windows-runtime-watch-pool.ts b/src/main/runtime/files/watch/windows-runtime-watch-pool.ts
new file mode 100644
index 00000000000..00aaa7a3390
--- /dev/null
+++ b/src/main/runtime/files/watch/windows-runtime-watch-pool.ts
@@ -0,0 +1,112 @@
+import type { FsChangeEvent } from '../../../../shared/filesystem-entry-types'
+import {
+  throwIfSignalAborted,
+  waitForPromiseWithSignal
+} from '../../../../shared/abort-signal-reason'
+import { normalizeRuntimePathForComparison } from '../../../../shared/cross-platform-path'
+import { isWatcherProcessFailure } from '../../../ipc/filesystem/watcher-process/parcel-watcher-process-failure'
+import { watchWindowsRuntimeFileExplorer } from './windows-file-watch'
+
+type Subscriber = {
+  onEvents: (events: FsChangeEvent[]) => void
+  onError: (error: Error) => void
+}
+
+type WindowsRootWatch = {
+  subscribers: Set<Subscriber>
+  close: () => Promise<void>
+  closing: Promise<void> | null
+  closeError: Error | null
+}
+
+export class WindowsRuntimeWatchPool {
+  private readonly roots = new Map<string, WindowsRootWatch>()
+
+  async watch(
+    rootPath: string,
+    onEvents: Subscriber['onEvents'],
+    onError: Subscriber['onError'],
+    signal?: AbortSignal
+  ): Promise<() => Promise<void>> {
+    throwIfSignalAborted(signal)
+    const key = normalizeRuntimePathForComparison(rootPath)
+    let root = this.roots.get(key)
+    if (root?.closing) {
+      await waitForPromiseWithSignal(root.closing, signal)
+      return this.watch(rootPath, onEvents, onError, signal)
+    }
+    if (root?.closeError) {
+      throw root.closeError
+    }
+    if (!root) {
+      root = this.createRoot(key, rootPath)
+      this.roots.set(key, root)
+    }
+    const ownedRoot = root
+    const subscriber = { onEvents, onError }
+    ownedRoot.subscribers.add(subscriber)
+    let releasePromise: Promise<void> | undefined
+    return () => {
+      if (releasePromise) {
+        return releasePromise
+      }
+      ownedRoot.subscribers.delete(subscriber)
+      if (ownedRoot.subscribers.size > 0) {
+        return Promise.resolve()
+      }
+      const attempt = this.closeRoot(key, ownedRoot)
+      releasePromise = attempt
+      void attempt.catch(() => {
+        releasePromise = undefined
+      })
+      return attempt
+    }
+  }
+
+  private createRoot(key: string, rootPath: string): WindowsRootWatch {
+    const subscribers = new Set<Subscriber>()
+    const close = watchWindowsRuntimeFileExplorer(
+      rootPath,
+      (events) => {
+        for (const subscriber of Array.from(subscribers)) {
+          if (subscribers.has(subscriber)) {
+            subscriber.onEvents(events)
+          }
+        }
+      },
+      (error) => {
+        if (this.roots.get(key)?.subscribers === subscribers) {
+          this.roots.delete(key)
+        }
+        const failedSubscribers = Array.from(subscribers)
+        subscribers.clear()
+        for (const subscriber of failedSubscribers) {
+          subscriber.onError(error)
+        }
+      }
+    )
+    return { subscribers, close, closing: null, closeError: null }
+  }
+
+  private closeRoot(key: string, root: WindowsRootWatch): Promise<void> {
+    if (root.closing) {
+      return root.closing
+    }
+    const forget = (): void => {
+      if (this.roots.get(key) === root) {
+        this.roots.delete(key)
+      }
+    }
+    const attempt = root.close().then(forget)
+    root.closing = attempt
+    void attempt.catch((error: unknown) => {
+      root.closeError = error instanceof Error ? error : new Error(String(error))
+      // A timed-out close still owns native locks until its physical exit.
+      root.closing =
+        isWatcherProcessFailure(error) && error.physicalExit
+          ? error.physicalExit.then(forget)
+          : null
+    })
+    return attempt
+  }
+}
diff --git a/src/main/runtime/orca-runtime-files-watch.test.ts b/src/main/runtime/orca-runtime-files-watch.test.ts
index b969bde0995..d23d07f883c 100644
--- a/src/main/runtime/orca-runtime-files-watch.test.ts
+++ b/src/main/runtime/orca-runtime-files-watch.test.ts
@@ -182,6 +182,38 @@ describe('RuntimeFileCommands file watching', () => {
     expect(settled).toBe(true)
   })
 
+  it('shares one Windows watch across clients without stopping survivors', async () => {
+    Object.defineProperty(process, 'platform', { configurable: true, value: 'win32' })
+    const watcher = createWindowsWatcher(() => watcher.emit('close'))
+    let emitChange = () => undefined
+    watchMock.mockImplementation((_rootPath, _options, callback) => {
+      emitChange = callback
+      return watcher
+    })
+    resolveAuthorizedPathMock.mockResolvedValue('C:\\repo')
+    statMock.mockResolvedValue({ isDirectory: () => true })
+    const { commands } = createRuntimeFileCommands('C:\\repo')
+    const callbacks = Array.from({ length: 2 }, () => vi.fn())
+    const releases = await Promise.all(
+      callbacks.map((callback) => commands.watchFileExplorer('id:wt-1', callback))
+    )
+    expect(watchMock).toHaveBeenCalledOnce()
+
+    await releases[0]()
+    expect(watcher.close).not.toHaveBeenCalled()
+    emitChange()
+    await vi.advanceTimersByTimeAsync(WINDOWS_RUNTIME_FILE_WATCH_LEADING_MS)
+    expect(callbacks[0]).not.toHaveBeenCalled()
+    for (const callback of callbacks.slice(1)) {
+      expect(callback).toHaveBeenCalledExactlyOnceWith([
+        { kind: 'overflow', absolutePath: 'C:\\repo' }
+      ])
+    }
+    await Promise.all(releases.slice(1).map((release) => release()))
+    expect(watcher.close).toHaveBeenCalledOnce()
+    expect(_getRuntimeFileWatcherReleaseCountForTests()).toBe(0)
+  })
+
   it('treats a Windows watcher error before cleanup as physical close', async () => {
     Object.defineProperty(process, 'platform', { configurable: true, value: 'win32' })
     const watcher = createWindowsWatcher(() => undefined)