diff --git a/apps/desktop/electron/main.ts b/apps/desktop/electron/main.ts
index 5f6edbe42c1..433320f370e 100644
--- a/apps/desktop/electron/main.ts
+++ b/apps/desktop/electron/main.ts
@@ -10868,7 +10868,12 @@ ipcMain.handle('hermes:fs:openDir', async (_event, dirPath) => {
 // on-disk plugin door silently breaks (#66899). Electron owns this resolution
 // so it stays valid in every connection mode. Created on demand, like openDir.
 ipcMain.handle('hermes:fs:desktopPluginsRoot', async () => {
-  const dir = path.join(HERMES_HOME, 'desktop-plugins')
+  // Profile-aware: a named Desktop profile gets its own plugin root under
+  // profiles/<name>/, matching the profile-scoped hermes_home the backend
+  // reported before this resolver existed. 'default'/unset pins the global root.
+  const profile = readActiveDesktopProfile()
+  const base = profile && profile !== 'default' ? path.join(HERMES_HOME, 'profiles', profile) : HERMES_HOME
+  const dir = path.join(base, 'desktop-plugins')
 
   try {
     await fs.promises.mkdir(dir, { recursive: true })
diff --git a/apps/desktop/src/contrib/runtime-loader.test.ts b/apps/desktop/src/contrib/runtime-loader.test.ts
index 253dc9e6822..cc1d4336c2d 100644
--- a/apps/desktop/src/contrib/runtime-loader.test.ts
+++ b/apps/desktop/src/contrib/runtime-loader.test.ts
@@ -3,7 +3,7 @@ import { afterEach, beforeEach, describe, expect, it, vi } from 'vitest'
 import type { HermesReadDirResult } from '@/global'
 import type * as HermesModule from '@/hermes'
 
-import { discoverRuntimePlugins } from './runtime-loader'
+import { discoverRuntimePlugins, watchRuntimePlugins } from './runtime-loader'
 
 // getStatus would supply the connected backend's hermes_home — a REMOTE path in
 // remote mode. The disk scanner must NOT derive the plugin root from it (#66899).
@@ -16,12 +16,21 @@ vi.mock('@/hermes', async importActual => ({
 
 const desktopPluginsRoot = vi.fn<() => Promise<string>>()
 const readDir = vi.fn<(path: string) => Promise<HermesReadDirResult>>()
+const watchDirectory = vi.fn<(path: string) => Promise<{ id: string }>>()
+const onPreviewFileChanged = vi.fn()
 
 beforeEach(() => {
   desktopPluginsRoot.mockReset()
   readDir.mockReset()
+  watchDirectory.mockReset()
+  onPreviewFileChanged.mockReset()
   getStatus.mockClear()
-  ;(window as unknown as { hermesDesktop: unknown }).hermesDesktop = { desktopPluginsRoot, readDir }
+  ;(window as unknown as { hermesDesktop: unknown }).hermesDesktop = {
+    desktopPluginsRoot,
+    onPreviewFileChanged,
+    readDir,
+    watchDirectory
+  }
 })
 
 afterEach(() => {
@@ -50,3 +59,19 @@ describe('scanDiskPlugins (#66899)', () => {
     expect(readDir).not.toHaveBeenCalled()
   })
 })
+
+describe('watchRuntimePlugins dir watch (#66899)', () => {
+  it('watches the Electron-resolved local root, never the backend hermes_home', async () => {
+    desktopPluginsRoot.mockResolvedValue('/local/.hermes/desktop-plugins')
+    readDir.mockResolvedValue({ entries: [] })
+    watchDirectory.mockResolvedValue({ id: 'watch-1' })
+
+    watchRuntimePlugins()
+    // Drain the async scan + startDirWatch chains.
+    await vi.waitFor(() => expect(watchDirectory).toHaveBeenCalled())
+
+    expect(watchDirectory).toHaveBeenCalledWith('/local/.hermes/desktop-plugins')
+    expect(watchDirectory).not.toHaveBeenCalledWith('/remote/box/.hermes/desktop-plugins')
+    expect(getStatus).not.toHaveBeenCalled()
+  })
+})
diff --git a/apps/desktop/src/contrib/runtime-loader.ts b/apps/desktop/src/contrib/runtime-loader.ts
index 1ae48fd0e16..27e6e40b95e 100644
--- a/apps/desktop/src/contrib/runtime-loader.ts
+++ b/apps/desktop/src/contrib/runtime-loader.ts
@@ -350,8 +350,15 @@ export function watchRuntimePlugins(): void {
     }
 
     try {
-      const { hermes_home } = await getStatus()
-      dirWatchId = (await desktop.watchDirectory(`${hermes_home}/desktop-plugins`)).id
+      // Same Electron-local root as the scanner — never the backend's
+      // hermes_home, which is a remote path in remote mode (#66899).
+      const root = await desktop.desktopPluginsRoot?.()
+
+      if (!root) {
+        return false
+      }
+
+      dirWatchId = (await desktop.watchDirectory(root)).id
 
       return true
     } catch {