diff --git a/packages/next/src/server/async-storage/request-async-storage-wrapper.ts b/packages/next/src/server/async-storage/request-async-storage-wrapper.ts
index 833b3ad1e0392..634e4c13be2ee 100644
--- a/packages/next/src/server/async-storage/request-async-storage-wrapper.ts
+++ b/packages/next/src/server/async-storage/request-async-storage-wrapper.ts
@@ -17,9 +17,9 @@ import {
   RequestCookiesAdapter,
   type ReadonlyRequestCookies,
 } from '../web/spec-extension/adapters/request-cookies'
-import type { ResponseCookies } from '../web/spec-extension/cookies'
-import { RequestCookies } from '../web/spec-extension/cookies'
+import { ResponseCookies, RequestCookies } from '../web/spec-extension/cookies'
 import { DraftModeProvider } from './draft-mode-provider'
+import { splitCookiesString } from '../web/utils'
 
 function getHeaders(headers: Headers | IncomingHttpHeaders): ReadonlyHeaders {
   const cleaned = HeadersAdapter.from(headers)
@@ -30,13 +30,6 @@ function getHeaders(headers: Headers | IncomingHttpHeaders): ReadonlyHeaders {
   return HeadersAdapter.seal(cleaned)
 }
 
-function getCookies(
-  headers: Headers | IncomingHttpHeaders
-): ReadonlyRequestCookies {
-  const cookies = new RequestCookies(HeadersAdapter.from(headers))
-  return RequestCookiesAdapter.seal(cookies)
-}
-
 function getMutableCookies(
   headers: Headers | IncomingHttpHeaders,
   onUpdateCookies?: (cookies: string[]) => void
@@ -103,24 +96,32 @@ export const RequestAsyncStorageWrapper: AsyncStorageWrapper<
         if (!cache.cookies) {
           // if middleware is setting cookie(s), then include those in
           // the initial cached cookies so they can be read in render
-          let combinedCookies
+          const requestCookies = new RequestCookies(
+            HeadersAdapter.from(req.headers)
+          )
+
           if (
             'x-middleware-set-cookie' in req.headers &&
             typeof req.headers['x-middleware-set-cookie'] === 'string'
           ) {
-            combinedCookies = `${req.headers.cookie}; ${req.headers['x-middleware-set-cookie']}`
+            const setCookieValue = req.headers['x-middleware-set-cookie']
+            const responseHeaders = new Headers()
+
+            for (const cookie of splitCookiesString(setCookieValue)) {
+              responseHeaders.append('set-cookie', cookie)
+            }
+
+            const responseCookies = new ResponseCookies(responseHeaders)
+
+            // Transfer cookies from ResponseCookies to RequestCookies
+            for (const cookie of responseCookies.getAll()) {
+              requestCookies.set(cookie.name, cookie.value ?? '')
+            }
           }
 
           // Seal the cookies object that'll freeze out any methods that could
           // mutate the underlying data.
-          cache.cookies = getCookies(
-            combinedCookies
-              ? {
-                  ...req.headers,
-                  cookie: combinedCookies,
-                }
-              : req.headers
-          )
+          cache.cookies = RequestCookiesAdapter.seal(requestCookies)
         }
 
         return cache.cookies
diff --git a/packages/next/src/server/web/spec-extension/cookies.ts b/packages/next/src/server/web/spec-extension/cookies.ts
index bfa953c5c9e8c..1fd37f5075b2b 100644
--- a/packages/next/src/server/web/spec-extension/cookies.ts
+++ b/packages/next/src/server/web/spec-extension/cookies.ts
@@ -1,4 +1,5 @@
 export {
   RequestCookies,
   ResponseCookies,
+  stringifyCookie,
 } from 'next/dist/compiled/@edge-runtime/cookies'
diff --git a/packages/next/src/server/web/spec-extension/response.ts b/packages/next/src/server/web/spec-extension/response.ts
index c680c2117a191..0e855ef701de6 100644
--- a/packages/next/src/server/web/spec-extension/response.ts
+++ b/packages/next/src/server/web/spec-extension/response.ts
@@ -1,3 +1,4 @@
+import { stringifyCookie } from '../../web/spec-extension/cookies'
 import type { I18NConfig } from '../../config-shared'
 import { NextURL } from '../next-url'
 import { toNodeOutgoingHttpHeaders, validateURL } from '../utils'
@@ -55,7 +56,13 @@ export class NextResponse<Body = unknown> extends Response {
               const newHeaders = new Headers(headers)
 
               if (result instanceof ResponseCookies) {
-                headers.set('x-middleware-set-cookie', result.toString())
+                headers.set(
+                  'x-middleware-set-cookie',
+                  result
+                    .getAll()
+                    .map((cookie) => stringifyCookie(cookie))
+                    .join(',')
+                )
               }
 
               handleMiddlewareField(init, newHeaders)
diff --git a/test/e2e/app-dir/app-middleware/app-middleware.test.ts b/test/e2e/app-dir/app-middleware/app-middleware.test.ts
index 40a0d36d9baad..778bce5918ad9 100644
--- a/test/e2e/app-dir/app-middleware/app-middleware.test.ts
+++ b/test/e2e/app-dir/app-middleware/app-middleware.test.ts
@@ -140,10 +140,12 @@ createNextDescribe(
 
       const initialRandom1 = await browser.elementById('rsc-cookie-1').text()
       const initialRandom2 = await browser.elementById('rsc-cookie-2').text()
+      const totalCookies = await browser.elementById('total-cookies').text()
 
       // cookies were set in middleware, assert they are present and match the Math.random() pattern
       expect(initialRandom1).toMatch(/Cookie 1: \d+\.\d+/)
       expect(initialRandom2).toMatch(/Cookie 2: \d+\.\d+/)
+      expect(totalCookies).toBe('Total Cookie Length: 2')
 
       await browser.refresh()
 
diff --git a/test/e2e/app-dir/app-middleware/app/rsc-cookies-delete/page.js b/test/e2e/app-dir/app-middleware/app/rsc-cookies-delete/page.js
index 9bdfed8530e18..38245781cbd8d 100644
--- a/test/e2e/app-dir/app-middleware/app/rsc-cookies-delete/page.js
+++ b/test/e2e/app-dir/app-middleware/app/rsc-cookies-delete/page.js
@@ -8,6 +8,7 @@ export default function Page() {
     <div>
       <p id="rsc-cookie-1">Cookie 1: {rscCookie1}</p>
       <p id="rsc-cookie-2">Cookie 2: {rscCookie2}</p>
+      <p id="total-cookies">Total Cookie Length: {cookies().size}</p>
     </div>
   )
 }
diff --git a/test/e2e/app-dir/app-middleware/app/rsc-cookies/page.js b/test/e2e/app-dir/app-middleware/app/rsc-cookies/page.js
index ed72af4c6607c..12dde4cb1b1f1 100644
--- a/test/e2e/app-dir/app-middleware/app/rsc-cookies/page.js
+++ b/test/e2e/app-dir/app-middleware/app/rsc-cookies/page.js
@@ -9,6 +9,7 @@ export default function Page() {
     <div>
       <p id="rsc-cookie-1">Cookie 1: {rscCookie1}</p>
       <p id="rsc-cookie-2">Cookie 2: {rscCookie2}</p>
+      <p id="total-cookies">Total Cookie Length: {cookies().size}</p>
       <Link href="/rsc-cookies-delete">To Delete Cookies Route</Link>
     </div>
   )