diff --git a/packages/next/build/webpack/plugins/middleware-plugin.ts b/packages/next/build/webpack/plugins/middleware-plugin.ts
index 82b94f8b4101..6711ade2f916 100644
--- a/packages/next/build/webpack/plugins/middleware-plugin.ts
+++ b/packages/next/build/webpack/plugins/middleware-plugin.ts
@@ -46,12 +46,6 @@ interface EntryMetadata {
 }
 
 const NAME = 'MiddlewarePlugin'
-const middlewareManifest: MiddlewareManifest = {
-  sortedMiddleware: [],
-  middleware: {},
-  functions: {},
-  version: 2,
-}
 
 /**
  * Checks the value of usingIndirectEval and when it is a set of modules it
@@ -121,6 +115,12 @@ function getCreateAssets(params: {
 }) {
   const { compilation, metadataByEntry } = params
   return (assets: any) => {
+    const middlewareManifest: MiddlewareManifest = {
+      sortedMiddleware: [],
+      middleware: {},
+      functions: {},
+      version: 2,
+    }
     for (const entrypoint of compilation.entrypoints.values()) {
       if (!entrypoint.name) {
         continue
diff --git a/packages/next/server/dev/on-demand-entry-handler.ts b/packages/next/server/dev/on-demand-entry-handler.ts
index 1c752b7b296d..4784fcf4489f 100644
--- a/packages/next/server/dev/on-demand-entry-handler.ts
+++ b/packages/next/server/dev/on-demand-entry-handler.ts
@@ -649,12 +649,22 @@ export function onDemandEntryHandler({
           },
           onServer: () => {
             added.set(COMPILER_NAMES.server, addEntry(COMPILER_NAMES.server))
+            const edgeServerEntry = `${COMPILER_NAMES.edgeServer}${pagePathData.page}`
+            if (entries[edgeServerEntry]) {
+              // Runtime switched from edge to server
+              delete entries[edgeServerEntry]
+            }
           },
           onEdgeServer: () => {
             added.set(
               COMPILER_NAMES.edgeServer,
               addEntry(COMPILER_NAMES.edgeServer)
             )
+            const serverEntry = `${COMPILER_NAMES.server}${pagePathData.page}`
+            if (entries[serverEntry]) {
+              // Runtime switched from server to edge
+              delete entries[serverEntry]
+            }
           },
         })
 
diff --git a/test/e2e/switchable-runtime/index.test.ts b/test/e2e/switchable-runtime/index.test.ts
index b9cef7819887..5485116ebc5c 100644
--- a/test/e2e/switchable-runtime/index.test.ts
+++ b/test/e2e/switchable-runtime/index.test.ts
@@ -203,6 +203,190 @@ describe('Switchable runtime', () => {
         }
       })
 
+      it('should be possible to switch between runtimes in API routes', async () => {
+        await check(
+          () => renderViaHTTP(next.url, '/api/switch-in-dev'),
+          'server response'
+        )
+
+        // Edge
+        await next.patchFile(
+          'pages/api/switch-in-dev.js',
+          `
+          export const config = {
+            runtime: 'experimental-edge',
+          }
+  
+          export default () => new Response('edge response')
+          `
+        )
+        await check(
+          () => renderViaHTTP(next.url, '/api/switch-in-dev'),
+          'edge response'
+        )
+
+        // Server
+        await next.patchFile(
+          'pages/api/switch-in-dev.js',
+          `
+          export default function (req, res) {
+            res.send('server response again')
+          }
+          `
+        )
+        await check(
+          () => renderViaHTTP(next.url, '/api/switch-in-dev'),
+          'server response again'
+        )
+
+        // Edge
+        await next.patchFile(
+          'pages/api/switch-in-dev.js',
+          `
+          export const config = {
+            runtime: 'experimental-edge',
+          }
+  
+          export default () => new Response('edge response again')
+          `
+        )
+        await check(
+          () => renderViaHTTP(next.url, '/api/switch-in-dev'),
+          'edge response again'
+        )
+      })
+
+      it('should be possible to switch between runtimes in pages', async () => {
+        await check(
+          () => renderViaHTTP(next.url, '/switch-in-dev'),
+          /Hello from edge page/
+        )
+
+        // Server
+        await next.patchFile(
+          'pages/switch-in-dev.js',
+          `
+          export default function Page() {
+            return <p>Hello from server page</p>
+          }
+          `
+        )
+        await check(
+          () => renderViaHTTP(next.url, '/switch-in-dev'),
+          /Hello from server page/
+        )
+
+        // Edge
+        await next.patchFile(
+          'pages/switch-in-dev.js',
+          `
+      export default function Page() {
+        return <p>Hello from edge page again</p>
+      }
+
+      export const config = {
+        runtime: 'experimental-edge',
+      }
+      `
+        )
+        await check(
+          () => renderViaHTTP(next.url, '/switch-in-dev'),
+          /Hello from edge page again/
+        )
+
+        // Server
+        await next.patchFile(
+          'pages/switch-in-dev.js',
+          `
+            export default function Page() {
+              return <p>Hello from server page again</p>
+            }
+            `
+        )
+        await check(
+          () => renderViaHTTP(next.url, '/switch-in-dev'),
+          /Hello from server page again/
+        )
+      })
+
+      // Doesn't work, see https://github.com/vercel/next.js/pull/39327
+      it.skip('should be possible to switch between runtimes with same content', async () => {
+        const fileContent = await next.readFile(
+          'pages/api/switch-in-dev-same-content.js'
+        )
+        console.log({ fileContent })
+        await check(
+          () => renderViaHTTP(next.url, '/api/switch-in-dev-same-content'),
+          'server response'
+        )
+
+        // Edge
+        await next.patchFile(
+          'pages/api/switch-in-dev-same-content.js',
+          `
+          export const config = {
+            runtime: 'experimental-edge',
+          }
+  
+          export default () => new Response('edge response')
+          `
+        )
+        await check(
+          () => renderViaHTTP(next.url, '/api/switch-in-dev-same-content'),
+          'edge response'
+        )
+
+        // Server - same content as first compilation of the server runtime version
+        await next.patchFile(
+          'pages/api/switch-in-dev-same-content.js',
+          fileContent
+        )
+        await check(
+          () => renderViaHTTP(next.url, '/api/switch-in-dev-same-content'),
+          'server response'
+        )
+      })
+
+      it('should recover from syntax error when using edge runtime', async () => {
+        await check(
+          () => renderViaHTTP(next.url, '/api/syntax-error-in-dev'),
+          'edge response'
+        )
+
+        // Syntax error
+        await next.patchFile(
+          'pages/api/syntax-error-in-dev.js',
+          `
+        export const config = {
+          runtime: 'experimental-edge',
+        }
+    
+        export default  => new Response('edge response')
+        `
+        )
+        await check(
+          () => renderViaHTTP(next.url, '/api/syntax-error-in-dev'),
+          /Unexpected token/
+        )
+
+        // Fix syntax error
+        await next.patchFile(
+          'pages/api/syntax-error-in-dev.js',
+          `
+          export default () => new Response('edge response again')
+
+          export const config = {
+            runtime: 'experimental-edge',
+          }
+          
+        `
+        )
+        await check(
+          () => renderViaHTTP(next.url, '/api/syntax-error-in-dev'),
+          'edge response again'
+        )
+      })
+
       it('should not crash the dev server when invalid runtime is configured', async () => {
         await check(
           () => renderViaHTTP(next.url, '/invalid-runtime'),
diff --git a/test/e2e/switchable-runtime/pages/api/switch-in-dev-same-content.js b/test/e2e/switchable-runtime/pages/api/switch-in-dev-same-content.js
new file mode 100644
index 000000000000..a587c8cb1a71
--- /dev/null
+++ b/test/e2e/switchable-runtime/pages/api/switch-in-dev-same-content.js
@@ -0,0 +1,3 @@
+export default (req, res) => {
+  res.send('server response')
+}
diff --git a/test/e2e/switchable-runtime/pages/api/switch-in-dev.js b/test/e2e/switchable-runtime/pages/api/switch-in-dev.js
new file mode 100644
index 000000000000..a587c8cb1a71
--- /dev/null
+++ b/test/e2e/switchable-runtime/pages/api/switch-in-dev.js
@@ -0,0 +1,3 @@
+export default (req, res) => {
+  res.send('server response')
+}
diff --git a/test/e2e/switchable-runtime/pages/api/syntax-error-in-dev.js b/test/e2e/switchable-runtime/pages/api/syntax-error-in-dev.js
new file mode 100644
index 000000000000..3b7243a1205e
--- /dev/null
+++ b/test/e2e/switchable-runtime/pages/api/syntax-error-in-dev.js
@@ -0,0 +1,5 @@
+export default () => new Response('edge response')
+
+export const config = {
+  runtime: `experimental-edge`,
+}
diff --git a/test/e2e/switchable-runtime/pages/switch-in-dev.js b/test/e2e/switchable-runtime/pages/switch-in-dev.js
new file mode 100644
index 000000000000..b67d4cabd53c
--- /dev/null
+++ b/test/e2e/switchable-runtime/pages/switch-in-dev.js
@@ -0,0 +1,7 @@
+export default function Page() {
+  return <p>Hello from edge page</p>
+}
+
+export const config = {
+  runtime: 'experimental-edge',
+}