diff --git a/src/build/vite/dev.ts b/src/build/vite/dev.ts
index 52682b009e..14509ee84a 100644
--- a/src/build/vite/dev.ts
+++ b/src/build/vite/dev.ts
@@ -6,7 +6,7 @@ import type { RunnerRPCHooks, UpgradeContext } from "env-runner";
 import { IncomingMessage, ServerResponse } from "node:http";
 import { NodeRequest, sendNodeResponse } from "srvx/node";
 import { createViteHotChannel } from "env-runner/vite";
-import { basename, dirname, join, normalize } from "pathe";
+import { basename, dirname, isAbsolute, join, normalize, relative } from "pathe";
 import { debounce } from "perfect-debounce";
 import { withBase, withoutBase } from "ufo";
 import { scanHandlers } from "../../scan.ts";
@@ -250,7 +250,8 @@ export async function configureViteDevServer(ctx: NitroPluginContext, server: Vi
   nitroEnv.devServer.onMessage(async (message: any) => {
     if (message?.__rpc === "transformHTML") {
       try {
-        const html = (await server.transformIndexHtml("/", message.data)).replace(
+        const htmlURL = _htmlTemplateURL(nitro.options.renderer?.template, server.config.root);
+        const html = (await server.transformIndexHtml(htmlURL, message.data)).replace(
           "<!--ssr-outlet-->",
           `{{{ globalThis.__nitro_vite_envs__?.["ssr"]?.fetch($REQUEST) || "" }}}`
         );
@@ -444,3 +445,12 @@ export function matchesMiddlewareRoute(route: string | undefined, url: string):
   const boundary = path[route.length];
   return !boundary || boundary === "/" || boundary === ".";
 }
+
+// Vite derives the HTML file path from the URL, which relative imports (e.g. in inline `<style>`) resolve against.
+function _htmlTemplateURL(template: string | undefined, root: string): string {
+  if (!template) {
+    return "/index.html";
+  }
+  const path = relative(root, template);
+  return path.startsWith("../") || isAbsolute(path) ? join("/@fs", template) : `/${path}`;
+}
diff --git a/test/vite/html-template-fixture/index.html b/test/vite/html-template-fixture/index.html
new file mode 100644
index 0000000000..eccaff29ea
--- /dev/null
+++ b/test/vite/html-template-fixture/index.html
@@ -0,0 +1,11 @@
+<!doctype html>
+<html>
+  <head>
+    <style>
+      @import "./src/style.css";
+    </style>
+  </head>
+  <body>
+    <h1>html template</h1>
+  </body>
+</html>
diff --git a/test/vite/html-template-fixture/src/style.css b/test/vite/html-template-fixture/src/style.css
new file mode 100644
index 0000000000..e9a20421be
--- /dev/null
+++ b/test/vite/html-template-fixture/src/style.css
@@ -0,0 +1,3 @@
+.imported-style {
+  color: rebeccapurple;
+}
diff --git a/test/vite/html-template-fixture/vite.config.ts b/test/vite/html-template-fixture/vite.config.ts
new file mode 100644
index 0000000000..dc884054e6
--- /dev/null
+++ b/test/vite/html-template-fixture/vite.config.ts
@@ -0,0 +1,6 @@
+import { defineConfig } from "vite";
+import { nitro } from "nitro/vite";
+
+export default defineConfig({
+  plugins: [nitro()],
+});
diff --git a/test/vite/html-template.test.ts b/test/vite/html-template.test.ts
new file mode 100644
index 0000000000..8fe7b91b0d
--- /dev/null
+++ b/test/vite/html-template.test.ts
@@ -0,0 +1,39 @@
+import { fileURLToPath } from "node:url";
+import type { ViteDevServer } from "vite";
+import { beforeAll, afterAll, describe, expect, test } from "vitest";
+
+const { createServer } = (await import(
+  process.env.NITRO_VITE_PKG || "vite"
+)) as typeof import("vite");
+
+describe("vite:html template", () => {
+  let server: ViteDevServer;
+  let serverURL: string;
+
+  const rootDir = fileURLToPath(new URL("./html-template-fixture", import.meta.url));
+
+  beforeAll(async () => {
+    server = await createServer({ root: rootDir, logLevel: "warn" });
+    await server.listen("0" as unknown as number);
+    const addr = server.httpServer?.address() as {
+      port: number;
+      address: string;
+      family: string;
+    };
+    serverURL = `http://${addr.family === "IPv6" ? `[${addr.address}]` : addr.address}:${addr.port}`;
+  }, 30_000);
+
+  afterAll(async () => {
+    await server?.close();
+  });
+
+  // Relative imports in inline `<style>` resolve against the template file, not the root dir.
+  test("resolves relative imports in inline styles", async () => {
+    const res = await fetch(serverURL, { headers: { accept: "text/html" } });
+    expect(res.status).toBe(200);
+    const html = await res.text();
+    expect(html).toContain("<h1>html template</h1>");
+    expect(html).toContain("rebeccapurple");
+    expect(html).not.toContain('@import "./src/style.css"');
+  });
+});