diff --git a/src/core/dev-server/server.ts b/src/core/dev-server/server.ts
index 7fd90cef37..0007726020 100644
--- a/src/core/dev-server/server.ts
+++ b/src/core/dev-server/server.ts
@@ -22,6 +22,7 @@ import type {
   Nitro,
   NitroBuildInfo,
   NitroDevServer,
+  NitroRouteRules,
   NitroWorker,
 } from "nitropack/types";
 import { resolve } from "pathe";
@@ -31,6 +32,8 @@ import serveStatic from "serve-static";
 import { joinURL } from "ufo";
 import defaultErrorHandler from "./error";
 import { createVFSHandler } from "./vfs";
+import { createRouter as createRadixRouter, toRouteMatcher } from "radix3";
+import defu from "defu";
 
 function initWorker(filename: string): Promise<NitroWorker> | undefined {
   if (!existsSync(filename)) {
@@ -166,13 +169,40 @@ export function createDevServer(nitro: Nitro): NitroDevServer {
   // Debugging endpoint to view vfs
   app.use("/_vfs", createVFSHandler(nitro));
 
+  // Apply headers based on routeRules. In cases where the dev server is being
+  // used, these would otherwise fail to be applied to public assets.
+  const routeRulesMatcher = toRouteMatcher(
+    createRadixRouter({ routes: nitro.options.routeRules })
+  );
   // Serve asset dirs
   for (const asset of nitro.options.publicAssets) {
     const url = joinURL(
       nitro.options.runtimeConfig.app.baseURL,
       asset.baseURL || "/"
     );
-    app.use(url, fromNodeMiddleware(serveStatic(asset.dir)));
+    app.use(
+      url,
+      fromNodeMiddleware(
+        serveStatic(asset.dir, {
+          setHeaders: (res) => {
+            const path = res.req.url;
+            if (path === undefined) {
+              return;
+            }
+            const rules: NitroRouteRules = defu(
+              {},
+              ...routeRulesMatcher.matchAll(path).reverse()
+            );
+            if (!rules.headers) {
+              return;
+            }
+            for (const [k, v] of Object.entries(rules.headers)) {
+              res.appendHeader(k, v);
+            }
+          },
+        })
+      )
+    );
     if (!asset.fallthrough) {
       app.use(url, fromNodeMiddleware(servePlaceholder()));
     }
diff --git a/test/fixture/nitro.config.ts b/test/fixture/nitro.config.ts
index 63d8eca4cd..1d0a985530 100644
--- a/test/fixture/nitro.config.ts
+++ b/test/fixture/nitro.config.ts
@@ -91,6 +91,7 @@ export default defineNitroConfig({
     "/rules/_/cached/noncached": { cache: false, swr: false, isr: false },
     "/rules/_/cached/**": { swr: true },
     "/api/proxy/**": { proxy: "/api/echo" },
+    "/build/**": { headers: { "x-build-header": "works" } },
   },
   prerender: {
     crawlLinks: true,
diff --git a/test/presets/netlify-legacy.test.ts b/test/presets/netlify-legacy.test.ts
index 5de5771d7f..33e8ba4733 100644
--- a/test/presets/netlify-legacy.test.ts
+++ b/test/presets/netlify-legacy.test.ts
@@ -82,19 +82,20 @@ describe("nitro:preset:netlify-legacy", async () => {
         );
 
         expect(headers).toMatchInlineSnapshot(`
-        "/rules/headers
-          cache-control: s-maxage=60
-        /rules/cors
-          access-control-allow-origin: *
-          access-control-allow-methods: GET
-          access-control-allow-headers: *
-          access-control-max-age: 0
-        /rules/nested/*
-          x-test: test
-        /build/*
-          cache-control: public, max-age=3600, immutable
-        "
-      `);
+          "/rules/headers
+            cache-control: s-maxage=60
+          /rules/cors
+            access-control-allow-origin: *
+            access-control-allow-methods: GET
+            access-control-allow-headers: *
+            access-control-max-age: 0
+          /rules/nested/*
+            x-test: test
+          /build/*
+            cache-control: public, max-age=3600, immutable
+            x-build-header: works
+          "
+        `);
       });
       it("should write config.json", async () => {
         const config = await fsp
diff --git a/test/presets/netlify.test.ts b/test/presets/netlify.test.ts
index a74afb093b..54dc76705a 100644
--- a/test/presets/netlify.test.ts
+++ b/test/presets/netlify.test.ts
@@ -62,19 +62,20 @@ describe("nitro:preset:netlify", async () => {
         );
 
         expect(headers).toMatchInlineSnapshot(`
-        "/rules/headers
-          cache-control: s-maxage=60
-        /rules/cors
-          access-control-allow-origin: *
-          access-control-allow-methods: GET
-          access-control-allow-headers: *
-          access-control-max-age: 0
-        /rules/nested/*
-          x-test: test
-        /build/*
-          cache-control: public, max-age=3600, immutable
-        "
-      `);
+          "/rules/headers
+            cache-control: s-maxage=60
+          /rules/cors
+            access-control-allow-origin: *
+            access-control-allow-methods: GET
+            access-control-allow-headers: *
+            access-control-max-age: 0
+          /rules/nested/*
+            x-test: test
+          /build/*
+            cache-control: public, max-age=3600, immutable
+            x-build-header: works
+          "
+        `);
       });
 
       it("writes config.json", async () => {
diff --git a/test/presets/nitro-dev.test.ts b/test/presets/nitro-dev.test.ts
index 9c6c39c5b7..cb8aa2a260 100644
--- a/test/presets/nitro-dev.test.ts
+++ b/test/presets/nitro-dev.test.ts
@@ -28,6 +28,22 @@ describe("nitro:preset:nitro-dev", async () => {
         expect(data.keys).includes("src:nitro.config.ts");
       });
 
+      it("static asset headers", async () => {
+        const { headers } = await ctx.fetch("/build/test.txt");
+        expect(Object.fromEntries(headers)).toMatchObject({
+          "accept-ranges": "bytes",
+          "cache-control": "public, max-age=0",
+          "last-modified": expect.any(String),
+          etag: 'W/"7-18df5a508c5"',
+          "content-type": "text/plain; charset=UTF-8",
+          "content-length": "7",
+          date: expect.any(String),
+          connection: "keep-alive",
+          "keep-alive": "timeout=5",
+          "x-build-header": "works",
+        });
+      });
+
       describe("openAPI", () => {
         let spec: OpenAPI3;
         it("/_openapi.json", async () => {
diff --git a/test/presets/vercel.test.ts b/test/presets/vercel.test.ts
index 25ad76cfe2..902d806106 100644
--- a/test/presets/vercel.test.ts
+++ b/test/presets/vercel.test.ts
@@ -93,6 +93,7 @@ describe("nitro:preset:vercel", async () => {
               {
                 "headers": {
                   "cache-control": "public, max-age=3600, immutable",
+                  "x-build-header": "works",
                 },
                 "src": "/build/(.*)",
               },