diff --git a/.github/workflows/ci.yml b/.github/workflows/ci.yml
index bcb99e29bc..a96b553cf5 100644
--- a/.github/workflows/ci.yml
+++ b/.github/workflows/ci.yml
@@ -237,16 +237,24 @@ jobs:
               run: |
                   source ~/.nvm/nvm.sh;
                   nvm install 22;
+                  cd $HOST_PATH
                   RUNNER_TRACKING_ID="" && ( \
-                    nohup node \
-                      --experimental-strip-types \
-                      --experimental-transform-types \
-                      --import ./packages/meta/src/node-es-module-loader/register.mts \
-                      ./packages/playground/cli/src/cli.ts server \
-                      --port=$PORT \
-                      --mount="$HOST_PATH:/wordpress/$VERSION" \
-                      --quiet& \
-                    )
+                    nohup python3 -c "import http.server
+                  import socketserver
+                  from urllib.parse import unquote
+
+                  class PrefixHTTPRequestHandler(http.server.SimpleHTTPRequestHandler):
+                      def do_GET(self):
+                          if self.path.startswith('/${{ env.VERSION }}/'):
+                              self.path = self.path[len('/${{ env.VERSION }}'):]
+                          elif self.path == '/${{ env.VERSION }}':
+                              self.path = '/'
+                          super().do_GET()
+
+                  with socketserver.TCPServer(('127.0.0.1', ${{ env.PORT }}), PrefixHTTPRequestHandler) as httpd:
+                      httpd.serve_forever()
+                  "&
+                  );
             - name: Wait for the package server to be ready
               run: |
                   for i in {1..60}; do
diff --git a/packages/playground/cli/src/run-cli.ts b/packages/playground/cli/src/run-cli.ts
index 65e8decd8f..266bd411fc 100644
--- a/packages/playground/cli/src/run-cli.ts
+++ b/packages/playground/cli/src/run-cli.ts
@@ -341,6 +341,7 @@ export async function runCLI(args: RunCLIArgs): Promise<RunCLIServer> {
 	const fileLockManager = new FileLockManagerForNode(nativeFlockSync);
 
 	let wordPressReady = false;
+	let isFirstRequest = true;
 
 	logger.log('Starting a PHP server...');
 
@@ -537,6 +538,28 @@ export async function runCLI(args: RunCLIArgs): Promise<RunCLIServer> {
 					'WordPress is not ready yet'
 				);
 			}
+			// Clear the playground_auto_login_already_happened cookie on the first request.
+			// Otherwise the first Playground CLI server started on the machine will set it,
+			// all the subsequent runs will get the stale cookie, and the auto-login will
+			// assume they don't have to auto-login again.
+			if (isFirstRequest) {
+				isFirstRequest = false;
+				const headers: Record<string, string[]> = {
+					'Content-Type': ['text/plain'],
+					'Content-Length': ['0'],
+					Location: ['/'],
+				};
+				if (
+					request.headers?.['cookie']?.includes(
+						'playground_auto_login_already_happened'
+					)
+				) {
+					headers['Set-Cookie'] = [
+						'playground_auto_login_already_happened=1; Max-Age=0; Expires=Thu, 01 Jan 1970 00:00:00 GMT; Path=/',
+					];
+				}
+				return new PHPResponse(302, headers, new Uint8Array());
+			}
 			return await loadBalancer.handleRequest(request);
 		},
 	});
diff --git a/packages/playground/cli/tests/test-running-unbuilt-cli.sh b/packages/playground/cli/tests/test-running-unbuilt-cli.sh
index bc13af4d5b..19037ced2d 100755
--- a/packages/playground/cli/tests/test-running-unbuilt-cli.sh
+++ b/packages/playground/cli/tests/test-running-unbuilt-cli.sh
@@ -30,7 +30,7 @@ function test_playground_cli() {
 		echo "Playground CLI started successfully"
 		echo "Checking WordPress home page..."
 
-		HOME_PAGE_OUTPUT="$(curl -s http://127.0.0.1:9400 || echo 'No output')"
+		HOME_PAGE_OUTPUT="$(curl -sL http://127.0.0.1:9400 || echo 'No output')"
 		if [[ $HOME_PAGE_OUTPUT != *"My WordPress Website"* ]]; then
 			echo "Home page output: $HOME_PAGE_OUTPUT"
 			echo "Error: Home page did not contain 'My WordPress Website'"
diff --git a/packages/playground/test-built-npm-packages/commonjs-and-jest/tests/wp.spec.ts b/packages/playground/test-built-npm-packages/commonjs-and-jest/tests/wp.spec.ts
index 677ec93a6d..d066cd2a43 100644
--- a/packages/playground/test-built-npm-packages/commonjs-and-jest/tests/wp.spec.ts
+++ b/packages/playground/test-built-npm-packages/commonjs-and-jest/tests/wp.spec.ts
@@ -22,6 +22,6 @@ SupportedPHPVersions.forEach((phpVersion: string) => {
 			} finally {
 				await cli[Symbol.asyncDispose]();
 			}
-		}, 10000);
+		}, 22000);
 	});
 });
diff --git a/packages/playground/test-built-npm-packages/es-modules-and-vitest/tests/wp.spec.ts b/packages/playground/test-built-npm-packages/es-modules-and-vitest/tests/wp.spec.ts
index f8db9886ce..1b6ea9d9f7 100644
--- a/packages/playground/test-built-npm-packages/es-modules-and-vitest/tests/wp.spec.ts
+++ b/packages/playground/test-built-npm-packages/es-modules-and-vitest/tests/wp.spec.ts
@@ -13,7 +13,7 @@ if (!SupportedPHPVersions.includes(phpVersion)) {
 }
 
 describe(`PHP ${phpVersion}`, () => {
-	it('Should load WordPress', { timeout: 12000 }, async () => {
+	it('Should load WordPress', { timeout: 22000 }, async () => {
 		const cli = await runCLI({
 			command: 'server',
 			php: phpVersion,