diff --git a/packages/dev/src/main.test.ts b/packages/dev/src/main.test.ts
index 2d0129d5..5fd13a89 100644
--- a/packages/dev/src/main.test.ts
+++ b/packages/dev/src/main.test.ts
@@ -1062,4 +1062,94 @@ describe('Handling requests', () => {
       await fixture.destroy()
     })
   })
+
+  describe('Static file serving', () => {
+    test('Serves static files from given `staticFiles.directories` only', async () => {
+      const fixture = new Fixture()
+        .withFile(
+          'netlify.toml',
+          `[build]
+        publish = "dist"
+        `,
+        )
+        .withFile('dist/index.html', `from dist`)
+        .withFile('custom-static/app.css', `from custom-static`)
+        .withFile('another-static/script.js', `from another-static`)
+      const directory = await fixture.create()
+
+      const dev = new NetlifyDev({
+        projectRoot: directory,
+        edgeFunctions: {},
+        geolocation: {
+          enabled: false,
+        },
+        staticFiles: {
+          directories: [`${directory}/custom-static`, `${directory}/another-static`],
+        },
+      })
+      await dev.start()
+
+      const customStaticRes = await dev.handle(new Request('https://site.netlify/app.css'))
+      expect(await customStaticRes?.text()).toBe('from custom-static')
+      const anotherStaticRes = await dev.handle(new Request('https://site.netlify/script.js'))
+      expect(await anotherStaticRes?.text()).toBe('from another-static')
+      const publishDirRes = await dev.handle(new Request('https://site.netlify/index.html'))
+      expect(publishDirRes).toBeUndefined()
+
+      await dev.stop()
+      await fixture.destroy()
+    })
+
+    test('Falls back to publish directory when no custom directories provided', async () => {
+      const fixture = new Fixture()
+        .withFile(
+          'netlify.toml',
+          `[build]
+        publish = "public"
+        `,
+        )
+        .withFile('public/index.html', `from public`)
+        .withFile('public/style.css', `from public css`)
+      const directory = await fixture.create()
+
+      const dev = new NetlifyDev({
+        projectRoot: directory,
+        edgeFunctions: {},
+        geolocation: {
+          enabled: false,
+        },
+      })
+      await dev.start()
+
+      const publishDirRes1 = await dev.handle(new Request('https://site.netlify/index.html'))
+      expect(await publishDirRes1?.text()).toBe('from public')
+      const publishDirRes2 = await dev.handle(new Request('https://site.netlify/style.css'))
+      expect(await publishDirRes2?.text()).toBe('from public css')
+
+      await dev.stop()
+      await fixture.destroy()
+    })
+
+    test('Uses project root when no publish directory configured and no custom directories provided', async () => {
+      const fixture = new Fixture().withFile('index.html', `from root`).withFile('app.js', `from root js`)
+      const directory = await fixture.create()
+
+      const dev = new NetlifyDev({
+        projectRoot: directory,
+        edgeFunctions: {},
+        geolocation: {
+          enabled: false,
+        },
+      })
+      await dev.start()
+
+      const projectRootRes1 = await dev.handle(new Request('https://site.netlify/index.html'))
+      expect(await projectRootRes1?.text()).toBe('from root')
+      const projectRootRes2 = await dev.handle(new Request('https://site.netlify/app.js'))
+      expect(await projectRootRes2?.text()).toBe('from root js')
+
+      await dev.stop()
+      await fixture.destroy()
+    })
+  })
 })
diff --git a/packages/dev/src/main.ts b/packages/dev/src/main.ts
index f85a8504..f86675da 100644
--- a/packages/dev/src/main.ts
+++ b/packages/dev/src/main.ts
@@ -123,8 +123,8 @@ export interface Features {
     enabled?: boolean
 
     /**
-     * Additional list of directories where static files can be found. The
-     * `publish` directory configured on your site will be used automatically.
+     * List of directories where static files can be found. If not provided,
+     * the `publish` directory configured on your Netlify project will be used automatically.
      */
     directories?: string[]
   }
@@ -196,7 +196,7 @@ export class NetlifyDev {
   #serverAddress?: string | null
   #siteID?: string
   #staticHandler?: StaticHandler
-  #staticHandlerAdditionalDirectories: string[]
+  #staticHandlerDirectories?: string[]
 
   constructor(options: NetlifyDevOptions) {
     if (options.apiURL) {
@@ -227,7 +227,7 @@ export class NetlifyDev {
     this.#logger = options.logger ?? globalThis.console
     this.#serverAddress = options.serverAddress
     this.#projectRoot = projectRoot
-    this.#staticHandlerAdditionalDirectories = options.staticFiles?.directories ?? []
+    this.#staticHandlerDirectories = options.staticFiles?.directories ?? undefined
   }
 
   private getServerAddress(requestServerAddress?: string) {
@@ -582,11 +582,12 @@ export class NetlifyDev {
     }
 
     if (this.#features.static) {
+      // If custom static directories are provided (e.g., by `@netlify/vite-plugin` or `@netlify/nuxt`),
+      // use those directories. Otherwise, use the build.publish directory from config.
+      const directories = this.#staticHandlerDirectories ?? [this.#config?.config.build.publish ?? this.#projectRoot]
+
       this.#staticHandler = new StaticHandler({
-        directory: [
-          this.#config?.config.build.publish ?? this.#projectRoot,
-          ...this.#staticHandlerAdditionalDirectories,
-        ],
+        directory: directories,
       })
     }