diff --git a/packages/nuxt/src/core/runtime/nitro/renderer.ts b/packages/nuxt/src/core/runtime/nitro/renderer.ts
index 98cfba67fc4..085e5564c22 100644
--- a/packages/nuxt/src/core/runtime/nitro/renderer.ts
+++ b/packages/nuxt/src/core/runtime/nitro/renderer.ts
@@ -30,7 +30,9 @@ interface RenderResult {
 }
 
 // @ts-ignore
-const getClientManifest = () => import('#build/dist/server/client.manifest.mjs').then(r => r.default || r)
+const getClientManifest = () => import('#build/dist/server/client.manifest.mjs')
+  .then(r => r.default || r)
+  .then(r => typeof r === 'function' ? r() : r)
 
 // @ts-ignore
 const getServerEntry = () => process.env.NUXT_NO_SSR ? Promise.resolve(null) : import('#build/dist/server/server.mjs').then(r => r.default || r)
@@ -46,15 +48,22 @@ const getSSRRenderer = lazyCachedFunction(async () => {
   if (!createSSRApp) { throw new Error('Server bundle is not available') }
 
   // Create renderer
-  const renderToString = async (input, context) => {
-    const html = await _renderToString(input, context)
-    return `<div id="__nuxt">${html}</div>`
-  }
-  return createRenderer(createSSRApp, {
+  const renderer = createRenderer(createSSRApp, {
     clientManifest,
     renderToString,
     publicPath: buildAssetsURL()
   })
+
+  async function renderToString (input, context) {
+    const html = await _renderToString(input, context)
+    // In development with vite-node, the manifest is on-demand and will be available after rendering
+    if (process.dev && process.env.NUXT_VITE_NODE_OPTIONS) {
+      renderer.rendererContext.updateManifest(await getClientManifest())
+    }
+    return `<div id="__nuxt">${html}</div>`
+  }
+
+  return renderer
 })
 
 // -- SPA Renderer --
diff --git a/packages/vite/src/runtime/client.manifest.mjs b/packages/vite/src/runtime/client.manifest.mjs
index f69d7371d26..f33e3b2a794 100644
--- a/packages/vite/src/runtime/client.manifest.mjs
+++ b/packages/vite/src/runtime/client.manifest.mjs
@@ -3,6 +3,4 @@ import { getViteNodeOptions } from './vite-node-shared.mjs'
 
 const viteNodeOptions = getViteNodeOptions()
 
-const manifest = await $fetch('/manifest', { baseURL: viteNodeOptions.baseURL })
-
-export default manifest
+export default () => $fetch('/manifest', { baseURL: viteNodeOptions.baseURL })