diff --git a/src/gateway/control-ui.http.test.ts b/src/gateway/control-ui.http.test.ts
index a2f2fe52fdb..c3693406962 100644
--- a/src/gateway/control-ui.http.test.ts
+++ b/src/gateway/control-ui.http.test.ts
@@ -180,6 +180,29 @@ describe("handleControlUiHttpRequest", () => {
     });
   });
 
+  it("serves HEAD for in-root assets without writing a body", async () => {
+    await withControlUiRoot({
+      fn: async (tmp) => {
+        const assetsDir = path.join(tmp, "assets");
+        await fs.mkdir(assetsDir, { recursive: true });
+        await fs.writeFile(path.join(assetsDir, "actual.txt"), "inside-ok\n");
+
+        const { res, end } = makeMockHttpResponse();
+        const handled = handleControlUiHttpRequest(
+          { url: "/assets/actual.txt", method: "HEAD" } as IncomingMessage,
+          res,
+          {
+            root: { kind: "resolved", path: tmp },
+          },
+        );
+
+        expect(handled).toBe(true);
+        expect(res.statusCode).toBe(200);
+        expect(end.mock.calls[0]?.length ?? -1).toBe(0);
+      },
+    });
+  });
+
   it("rejects symlinked SPA fallback index.html outside control-ui root", async () => {
     await withControlUiRoot({
       fn: async (tmp) => {
diff --git a/src/gateway/control-ui.ts b/src/gateway/control-ui.ts
index 08bc2500bb7..85a68caf86b 100644
--- a/src/gateway/control-ui.ts
+++ b/src/gateway/control-ui.ts
@@ -179,19 +179,21 @@ function respondNotFound(res: ServerResponse) {
   res.end("Not Found");
 }
 
-function serveFile(res: ServerResponse, filePath: string) {
+function setStaticFileHeaders(res: ServerResponse, filePath: string) {
   const ext = path.extname(filePath).toLowerCase();
   res.setHeader("Content-Type", contentTypeForExt(ext));
   // Static UI should never be cached aggressively while iterating; allow the
   // browser to revalidate.
   res.setHeader("Cache-Control", "no-cache");
+}
+
+function serveFile(res: ServerResponse, filePath: string) {
+  setStaticFileHeaders(res, filePath);
   res.end(fs.readFileSync(filePath));
 }
 
 function serveResolvedFile(res: ServerResponse, filePath: string, body: Buffer) {
-  const ext = path.extname(filePath).toLowerCase();
-  res.setHeader("Content-Type", contentTypeForExt(ext));
-  res.setHeader("Cache-Control", "no-cache");
+  setStaticFileHeaders(res, filePath);
   res.end(body);
 }
 
@@ -217,12 +219,11 @@ function areSameFileIdentity(preOpen: fs.Stats, opened: fs.Stats): boolean {
 }
 
 function resolveSafeControlUiFile(
-  root: string,
+  rootReal: string,
   filePath: string,
-): { path: string; body: Buffer } | null {
+): { path: string; fd: number } | null {
   let fd: number | null = null;
   try {
-    const rootReal = fs.realpathSync(root);
     const fileReal = fs.realpathSync(filePath);
     if (!isContainedPath(rootReal, fileReal)) {
       return null;
@@ -243,7 +244,9 @@ function resolveSafeControlUiFile(
       return null;
     }
 
-    return { path: fileReal, body: fs.readFileSync(fd) };
+    const resolved = { path: fileReal, fd };
+    fd = null;
+    return resolved;
   } catch (error) {
     if (isExpectedSafePathError(error)) {
       return null;
@@ -377,6 +380,25 @@ export function handleControlUiHttpRequest(
     return true;
   }
 
+  const rootReal = (() => {
+    try {
+      return fs.realpathSync(root);
+    } catch (error) {
+      if (isExpectedSafePathError(error)) {
+        return null;
+      }
+      throw error;
+    }
+  })();
+  if (!rootReal) {
+    res.statusCode = 503;
+    res.setHeader("Content-Type", "text/plain; charset=utf-8");
+    res.end(
+      "Control UI assets not found. Build them with `pnpm ui:build` (auto-installs UI deps), or run `pnpm ui:dev` during development.",
+    );
+    return true;
+  }
+
   const uiPath =
     basePath && pathname.startsWith(`${basePath}/`) ? pathname.slice(basePath.length) : pathname;
   const rel = (() => {
@@ -402,14 +424,24 @@ export function handleControlUiHttpRequest(
     return true;
   }
 
-  const safeFile = resolveSafeControlUiFile(root, filePath);
+  const safeFile = resolveSafeControlUiFile(rootReal, filePath);
   if (safeFile) {
-    if (path.basename(safeFile.path) === "index.html") {
-      serveResolvedIndexHtml(res, safeFile.body.toString("utf8"));
+    try {
+      if (req.method === "HEAD") {
+        res.statusCode = 200;
+        setStaticFileHeaders(res, safeFile.path);
+        res.end();
+        return true;
+      }
+      if (path.basename(safeFile.path) === "index.html") {
+        serveResolvedIndexHtml(res, fs.readFileSync(safeFile.fd, "utf8"));
+        return true;
+      }
+      serveResolvedFile(res, safeFile.path, fs.readFileSync(safeFile.fd));
       return true;
+    } finally {
+      fs.closeSync(safeFile.fd);
     }
-    serveResolvedFile(res, safeFile.path, safeFile.body);
-    return true;
   }
 
   // If the requested path looks like a static asset (known extension), return
@@ -424,10 +456,20 @@ export function handleControlUiHttpRequest(
 
   // SPA fallback (client-side router): serve index.html for unknown paths.
   const indexPath = path.join(root, "index.html");
-  const safeIndex = resolveSafeControlUiFile(root, indexPath);
+  const safeIndex = resolveSafeControlUiFile(rootReal, indexPath);
   if (safeIndex) {
-    serveResolvedIndexHtml(res, safeIndex.body.toString("utf8"));
-    return true;
+    try {
+      if (req.method === "HEAD") {
+        res.statusCode = 200;
+        setStaticFileHeaders(res, safeIndex.path);
+        res.end();
+        return true;
+      }
+      serveResolvedIndexHtml(res, fs.readFileSync(safeIndex.fd, "utf8"));
+      return true;
+    } finally {
+      fs.closeSync(safeIndex.fd);
+    }
   }
 
   respondNotFound(res);