diff --git a/packages/vite/src/node/server/__tests__/watcher.spec.ts b/packages/vite/src/node/server/__tests__/watcher.spec.ts
index 90b68fcfd88d0f..df0e8c0641d0d7 100644
--- a/packages/vite/src/node/server/__tests__/watcher.spec.ts
+++ b/packages/vite/src/node/server/__tests__/watcher.spec.ts
@@ -1,9 +1,47 @@
-import { describe, expect, it } from 'vitest'
+import { resolve } from 'node:path'
+import {
+  type MockInstance,
+  afterEach,
+  beforeEach,
+  describe,
+  expect,
+  it,
+  vi,
+} from 'vitest'
+import chokidar from 'chokidar'
 import { createServer } from '../index'
 
 const stubGetWatchedCode = /getWatched\(\) \{.+?return \{\};.+?\}/s
 
+let watchSpy: MockInstance<
+  Parameters<typeof chokidar.watch>,
+  ReturnType<typeof chokidar.watch>
+>
+
+vi.mock('../../config', async () => {
+  const config: typeof import('../../config') =
+    await vi.importActual('../../config')
+  const resolveConfig = config.resolveConfig
+  vi.spyOn(config, 'resolveConfig').mockImplementation(async (...args) => {
+    const resolved: Awaited<ReturnType<typeof resolveConfig>> =
+      await resolveConfig.call(config, ...args)
+    resolved.configFileDependencies.push(
+      resolve('fake/config/dependency.js').replace(/\\/g, '/'),
+    )
+    return resolved
+  })
+  return config
+})
+
 describe('watcher configuration', () => {
+  beforeEach(() => {
+    watchSpy = vi.spyOn(chokidar, 'watch')
+  })
+
+  afterEach(() => {
+    watchSpy.mockRestore()
+  })
+
   it('when watcher is disabled, return noop watcher', async () => {
     const server = await createServer({
       server: {
@@ -21,4 +59,27 @@ describe('watcher configuration', () => {
     })
     expect(server.watcher.getWatched.toString()).not.toMatch(stubGetWatchedCode)
   })
+
+  it('should watch the root directory, config file dependencies, dotenv files, and the public directory', async () => {
+    await createServer({
+      server: {
+        watch: {},
+      },
+      publicDir: '__test_public__',
+    })
+    expect(watchSpy).toHaveBeenLastCalledWith(
+      expect.arrayContaining(
+        [
+          process.cwd(),
+          resolve('fake/config/dependency.js'),
+          resolve('.env'),
+          resolve('.env.local'),
+          resolve('.env.development'),
+          resolve('.env.development.local'),
+          resolve('__test_public__'),
+        ].map((file) => file.replace(/\\/g, '/')),
+      ),
+      expect.anything(),
+    )
+  })
 })
diff --git a/packages/vite/src/node/server/index.ts b/packages/vite/src/node/server/index.ts
index c7a73456187938..964b8e37a85000 100644
--- a/packages/vite/src/node/server/index.ts
+++ b/packages/vite/src/node/server/index.ts
@@ -466,6 +466,9 @@ export async function _createServer(
     config.server.hmr.channels.forEach((channel) => hot.addChannel(channel))
   }
 
+  const publicFiles = await initPublicFilesPromise
+  const { publicDir } = config
+
   if (httpServer) {
     setClientErrorHandler(httpServer, config.logger)
   }
@@ -479,6 +482,9 @@ export async function _createServer(
           root,
           ...config.configFileDependencies,
           ...getEnvFilesForMode(config.mode, config.envDir),
+          // Watch the public directory explicitly because it might be outside
+          // of the root directory.
+          ...(publicDir && publicFiles ? [publicDir] : []),
         ],
         resolvedWatchOptions,
       ) as FSWatcher)
@@ -745,8 +751,6 @@ export async function _createServer(
     }
   }
 
-  const publicFiles = await initPublicFilesPromise
-
   const onHMRUpdate = async (
     type: 'create' | 'delete' | 'update',
     file: string,
@@ -763,8 +767,6 @@ export async function _createServer(
     }
   }
 
-  const { publicDir } = config
-
   const onFileAddUnlink = async (file: string, isUnlink: boolean) => {
     file = normalizePath(file)
     await container.watchChange(file, { event: isUnlink ? 'delete' : 'create' })