diff --git a/includes/http/GuzzleHttpRequest.php b/includes/http/GuzzleHttpRequest.php
index f857826e4a0..624c215740f 100644
--- a/includes/http/GuzzleHttpRequest.php
+++ b/includes/http/GuzzleHttpRequest.php
@@ -19,7 +19,10 @@
  */
 
 use GuzzleHttp\Client;
+use GuzzleHttp\HandlerStack;
+use GuzzleHttp\Middleware;
 use GuzzleHttp\Psr7\Request;
+use Psr\Http\Message\RequestInterface;
 
 /**
  * MWHttpRequest implemented using the Guzzle library
@@ -154,9 +157,32 @@ class GuzzleHttpRequest extends MWHttpRequest {
 
 		$this->guzzleOptions['headers'] = $this->reqHeaders;
 
-		if ( $this->handler ) {
-			$this->guzzleOptions['handler'] = $this->handler;
-		}
+		// Create Middleware to use cookies from $this->getCookieJar(),
+		// which is in MediaWiki CookieJar format, not in Guzzle-specific CookieJar format.
+		// Note: received cookies (from HTTP response) don't need to be handled here,
+		// they will be added back into the CookieJar by MWHttpRequest::parseCookies().
+		$stack = HandlerStack::create( $this->handler );
+
+		// @phan-suppress-next-line PhanUndeclaredFunctionInCallable
+		$stack->remove( 'cookies' );
+
+		$mwCookieJar = $this->getCookieJar();
+		$stack->push( Middleware::mapRequest(
+			function ( RequestInterface $request ) use ( $mwCookieJar ) {
+				$uri = $request->getUri();
+				$cookieHeader = $mwCookieJar->serializeToHttpRequest(
+					$uri->getPath() ?: '/',
+					$uri->getHost()
+				);
+				if ( !$cookieHeader ) {
+					return $request;
+				}
+
+				return $request->withHeader( 'Cookie', $cookieHeader );
+			}
+		), 'cookies' );
+
+		$this->guzzleOptions['handler'] = $stack;
 
 		if ( $this->sink ) {
 			$this->guzzleOptions['sink'] = $this->sink;
diff --git a/tests/phpunit/includes/http/GuzzleHttpRequestTest.php b/tests/phpunit/includes/http/GuzzleHttpRequestTest.php
index 8ae6d33f364..0f726973d19 100644
--- a/tests/phpunit/includes/http/GuzzleHttpRequestTest.php
+++ b/tests/phpunit/includes/http/GuzzleHttpRequestTest.php
@@ -156,7 +156,7 @@ class GuzzleHttpRequestTest extends MediaWikiTestCase {
 	public function testPostBody() {
 		$container = [];
 		$history = Middleware::history( $container );
-		$stack = HandlerStack::create();
+		$stack = HandlerStack::create( new MockHandler( [ new Response() ] ) );
 		$stack->push( $history );
 		$client = new GuzzleHttpRequest( $this->exampleUrl, [
 			'method' => 'POST',
@@ -170,4 +170,48 @@ class GuzzleHttpRequestTest extends MediaWikiTestCase {
 		$this->assertEquals( 'application/x-www-form-urlencoded',
 			$request->getHeader( 'Content-Type' )[0] );
 	}
+
+	/*
+	 * Test that cookies from CookieJar were sent in the outgoing request.
+	 */
+	public function testCookieSent() {
+		$domain = wfParseUrl( $this->exampleUrl )['host'];
+		$expectedCookies = [ 'cookie1' => 'value1', 'anothercookie' => 'secondvalue' ];
+		$jar = new CookieJar;
+		foreach ( $expectedCookies as $key => $val ) {
+			$jar->setCookie( $key, $val, [ 'domain' => $domain ] );
+		}
+
+		$container = [];
+		$history = Middleware::history( $container );
+		$stack = HandlerStack::create( new MockHandler( [ new Response() ] ) );
+		$stack->push( $history );
+		$client = new GuzzleHttpRequest( $this->exampleUrl, [
+			'method' => 'POST',
+			'handler' => $stack,
+			'post' => 'key=value',
+		] );
+		$client->setCookieJar( $jar );
+		$client->execute();
+
+		$request = $container[0]['request'];
+		$this->assertEquals( [ 'cookie1=value1; anothercookie=secondvalue' ],
+			$request->getHeader( 'Cookie' ) );
+	}
+
+	/*
+	 * Test that cookies returned by HTTP response were added back into the CookieJar.
+	 */
+	public function testCookieReceived() {
+		$handler = HandlerStack::create( new MockHandler( [ new Response( 200, [
+			'status' => 200,
+			'Set-Cookie' => [ 'cookie1=value1', 'anothercookie=secondvalue' ]
+		] ) ] ) );
+		$r = new GuzzleHttpRequest( $this->exampleUrl, [ 'handler' => $handler ] );
+		$r->execute();
+
+		$domain = wfParseUrl( $this->exampleUrl )['host'];
+		$this->assertEquals( 'cookie1=value1; anothercookie=secondvalue',
+			$r->getCookieJar()->serializeToHttpRequest( '/', $domain ) );
+	}
 }