diff --git a/packages/next/client/app-index.tsx b/packages/next/client/app-index.tsx
index 2e51e8277210..b7ca2b3d227a 100644
--- a/packages/next/client/app-index.tsx
+++ b/packages/next/client/app-index.tsx
@@ -169,7 +169,10 @@ function createLoadFlightCssStream(callback?: () => Promise<void>) {
   const loadCssFromStreamData = (data: string) => {
     if (data.startsWith('CSS')) {
       const cssJson = data.slice(4).trim()
-      if (!loadedCss.has(cssJson)) cssLoadingPromises.push(loadCss(cssJson))
+      if (!loadedCss.has(cssJson)) {
+        loadedCss.add(cssJson)
+        cssLoadingPromises.push(loadCss(cssJson))
+      }
     }
   }
 
@@ -177,23 +180,26 @@ function createLoadFlightCssStream(callback?: () => Promise<void>) {
   let buffer = ''
   const loadCssFromFlight = new TransformStream({
     transform(chunk, controller) {
+      const process = (buf: string) => {
+        if (buf) {
+          if (buf.startsWith('CSS:')) {
+            loadCssFromStreamData(buf)
+          } else {
+            controller.enqueue(new TextEncoder().encode(buf))
+          }
+        }
+      }
+
       const data = new TextDecoder().decode(chunk)
       buffer += data
       let index
       while ((index = buffer.indexOf('\n')) !== -1) {
         const line = buffer.slice(0, index + 1)
         buffer = buffer.slice(index + 1)
-        if (line.startsWith('CSS:')) {
-          loadCssFromStreamData(line)
-        } else {
-          controller.enqueue(new TextEncoder().encode(line))
-        }
-      }
-
-      if (buffer && !buffer.startsWith('CSS:')) {
-        controller.enqueue(new TextEncoder().encode(buffer))
-        buffer = ''
+        process(line)
       }
+      process(buffer)
+      buffer = ''
     },
   })
 
@@ -262,9 +268,7 @@ function RSCComponent(props: any) {
   return <ServerRoot {...props} cacheKey={cacheKey} />
 }
 
-export async function hydrate(opts?: {
-  onFlightCssLoaded?: () => Promise<void>
-}) {
+export function hydrate(opts?: { onFlightCssLoaded?: () => Promise<void> }) {
   renderReactElement(appElement!, () => (
     <React.StrictMode>
       <Root>
diff --git a/packages/next/client/components/app-router.client.tsx b/packages/next/client/components/app-router.client.tsx
index 9b571472108e..cd9d5b06a239 100644
--- a/packages/next/client/components/app-router.client.tsx
+++ b/packages/next/client/components/app-router.client.tsx
@@ -49,26 +49,26 @@ function fetchFlight(url: URL, flightRouterStateData: string): ReadableStream {
   let buffer = ''
   const loadCssFromFlight = new TransformStream({
     transform(chunk, controller) {
+      const process = (buf: string) => {
+        if (buf) {
+          if (buf.startsWith('CSS:')) {
+            loadCssFromStreamData(buf)
+          } else {
+            controller.enqueue(new TextEncoder().encode(buf))
+          }
+        }
+      }
+
       const data = new TextDecoder().decode(chunk)
       buffer += data
       let index
       while ((index = buffer.indexOf('\n')) !== -1) {
         const line = buffer.slice(0, index + 1)
         buffer = buffer.slice(index + 1)
-
-        if (line.startsWith('CSS:')) {
-          loadCssFromStreamData(line)
-        } else {
-          controller.enqueue(new TextEncoder().encode(line))
-        }
-      }
-      if (buffer && !buffer.startsWith('CSS:')) {
-        controller.enqueue(new TextEncoder().encode(buffer))
-        buffer = ''
+        process(line)
       }
-    },
-    flush() {
-      loadCssFromStreamData(buffer)
+      process(buffer)
+      buffer = ''
     },
   })
 
diff --git a/packages/next/server/app-render.tsx b/packages/next/server/app-render.tsx
index bd5109398f94..993495b9e6e6 100644
--- a/packages/next/server/app-render.tsx
+++ b/packages/next/server/app-render.tsx
@@ -191,7 +191,11 @@ function createServerComponentRenderer(
     globalThis.__next_chunk_load__ = () => Promise.resolve()
   }
 
-  const cssFlightData = getCssFlightData(ComponentMod, serverComponentManifest)
+  const cssFlightData = getCssFlightData(
+    ComponentMod,
+    serverComponentManifest,
+    dev
+  )
 
   let RSCStream: ReadableStream<Uint8Array>
   const createRSCStream = () => {
@@ -346,7 +350,11 @@ function getCSSInlinedLinkTags(
   )
 }
 
-function getCssFlightData(ComponentMod: any, serverComponentManifest: any) {
+function getCssFlightData(
+  ComponentMod: any,
+  serverComponentManifest: any,
+  dev: boolean
+) {
   const importedServerCSSFiles: string[] =
     ComponentMod.__client__?.__next_rsc_css__ || []
 
@@ -354,6 +362,11 @@ function getCssFlightData(ComponentMod: any, serverComponentManifest: any) {
     (css) => serverComponentManifest[css].default
   )
 
+  if (dev) {
+    // Keep `id` in dev mode css flight to require the css module
+    return cssFiles.map((css) => `CSS:${JSON.stringify(css)}`).join('\n') + '\n'
+  }
+
   // Multiple css chunks could be merged into one by mini-css-extract-plugin,
   // we use a set here to dedupe the css chunks in production.
   const cssSet: Set<string> = cssFiles.reduce((res, css) => {
@@ -781,7 +794,8 @@ export async function renderToHTML(
 
     const cssFlightData = getCssFlightData(
       ComponentMod,
-      serverComponentManifest
+      serverComponentManifest,
+      dev
     )
     const flightData: FlightData = [
       // TODO-APP: change walk to output without ''
diff --git a/packages/next/server/node-web-streams-helper.ts b/packages/next/server/node-web-streams-helper.ts
index 6502173af9ae..769df24adefd 100644
--- a/packages/next/server/node-web-streams-helper.ts
+++ b/packages/next/server/node-web-streams-helper.ts
@@ -231,9 +231,9 @@ export function createPrefixStream(
   let prefixFlushed = false
   return new TransformStream({
     transform(chunk, controller) {
-      if (!prefixFlushed && prefix) {
-        prefixFlushed = true
+      if (!prefixFlushed) {
         controller.enqueue(encodeText(prefix))
+        prefixFlushed = true
       }
       controller.enqueue(chunk)
     },