diff --git a/python/server/qgsserver.sip b/python/server/qgsserver.sip
index 9cf2f4e1b0f..adb3e2f2a20 100644
--- a/python/server/qgsserver.sip
+++ b/python/server/qgsserver.sip
@@ -35,7 +35,7 @@ class QgsServer
 .. versionadded:: 2.14
 %End
 
-    void handleRequest( QgsServerRequest &request, QgsServerResponse &response );
+    void handleRequest( QgsServerRequest &request, QgsServerResponse &response, const QgsProject *project = 0 );
 %Docstring
  Handles the request.
  The query string is normally read from environment
@@ -44,6 +44,9 @@ class QgsServer
 
  \param request a QgsServerRequest holding request parameters
  \param response a QgsServerResponse for handling response I/O)
+ \param project a QgsProject or None, if it is None the project
+        is created from the MAP param specified in request or from
+        the QGIS_PROJECT_FILE setting
 %End
 
 
diff --git a/src/server/qgsserver.cpp b/src/server/qgsserver.cpp
index d2a7b4f7443..dd47115012d 100644
--- a/src/server/qgsserver.cpp
+++ b/src/server/qgsserver.cpp
@@ -300,8 +300,7 @@ void QgsServer::putenv( const QString &var, const QString &val )
  * @param queryString
  * @return response headers and body
  */
-
-void QgsServer::handleRequest( QgsServerRequest &request, QgsServerResponse &response )
+void QgsServer::handleRequest( QgsServerRequest &request, QgsServerResponse &response, const QgsProject *project )
 {
   QgsMessageLog::MessageLevel logLevel = QgsServerLogger::instance()->logLevel();
   QTime time; //used for measuring request time if loglevel < 1
@@ -346,16 +345,23 @@ void QgsServer::handleRequest( QgsServerRequest &request, QgsServerResponse &res
       printRequestParameters( parameterMap, logLevel );
 
       //Config file path
-      QString configFilePath = configPath( *sConfigFilePath, parameterMap );
-
-      // load the project if needed and not empty
-      const QgsProject *project = mConfigCache->project( configFilePath );
       if ( ! project )
       {
-        throw QgsServerException( QStringLiteral( "Project file error" ) );
-      }
+        QString configFilePath = configPath( *sConfigFilePath, parameterMap );
 
-      sServerInterface->setConfigFilePath( configFilePath );
+        // load the project if needed and not empty
+        project = mConfigCache->project( configFilePath );
+        if ( ! project )
+        {
+          throw QgsServerException( QStringLiteral( "Project file error" ) );
+        }
+
+        sServerInterface->setConfigFilePath( configFilePath );
+      }
+      else
+      {
+        sServerInterface->setConfigFilePath( project->fileName() );
+      }
 
       //Service parameter
       QString serviceString = parameterMap.value( QStringLiteral( "SERVICE" ) );
diff --git a/src/server/qgsserver.h b/src/server/qgsserver.h
index 6f4ffd908bf..1ea88ed2b1d 100644
--- a/src/server/qgsserver.h
+++ b/src/server/qgsserver.h
@@ -75,8 +75,11 @@ class SERVER_EXPORT QgsServer
      *
      * \param request a QgsServerRequest holding request parameters
      * \param response a QgsServerResponse for handling response I/O)
+     * \param project a QgsProject or nullptr, if it is nullptr the project
+     *        is created from the MAP param specified in request or from
+     *        the QGIS_PROJECT_FILE setting
      */
-    void handleRequest( QgsServerRequest &request, QgsServerResponse &response );
+    void handleRequest( QgsServerRequest &request, QgsServerResponse &response, const QgsProject *project = nullptr );
 
 
     //! Returns a pointer to the server interface
diff --git a/tests/src/python/test_qgsserver.py b/tests/src/python/test_qgsserver.py
index c2c6edbc531..70568fd12f8 100644
--- a/tests/src/python/test_qgsserver.py
+++ b/tests/src/python/test_qgsserver.py
@@ -214,6 +214,17 @@ class QgsServerTestBase(unittest.TestCase):
             headers.append(("%s: %s" % (k, rh[k])).encode('utf-8'))
         return b"\n".join(headers) + b"\n\n", bytes(response.body())
 
+    def _execute_request_project(self, qs, project, requestMethod=QgsServerRequest.GetMethod, data=None):
+        request = QgsBufferServerRequest(qs, requestMethod, {}, data)
+        response = QgsBufferServerResponse()
+        self.server.handleRequest(request, response, project)
+        headers = []
+        rh = response.headers()
+        rk = sorted(rh.keys())
+        for k in rk:
+            headers.append(("%s: %s" % (k, rh[k])).encode('utf-8'))
+        return b"\n".join(headers) + b"\n\n", bytes(response.body())
+
 
 class TestQgsServerTestBase(unittest.TestCase):
 
@@ -285,6 +296,16 @@ class TestQgsServer(QgsServerTestBase):
         self.assertEqual(response.headers(), {'Content-Length': '54', 'Content-Type': 'text/xml; charset=utf-8'})
         self.assertEqual(response.statusCode(), 500)
 
+    def test_requestHandlerProject(self):
+        """Test request handler with none project"""
+        headers = {'header-key-1': 'header-value-1', 'header-key-2': 'header-value-2'}
+        request = QgsBufferServerRequest('http://somesite.com/somepath', QgsServerRequest.GetMethod, headers)
+        response = QgsBufferServerResponse()
+        self.server.handleRequest(request, response, None)
+        self.assertEqual(bytes(response.body()), b'<ServerException>Project file error</ServerException>\n')
+        self.assertEqual(response.headers(), {'Content-Length': '54', 'Content-Type': 'text/xml; charset=utf-8'})
+        self.assertEqual(response.statusCode(), 500)
+
     def test_api(self):
         """Using an empty query string (returns an XML exception)
         we are going to test if headers and body are returned correctly"""
diff --git a/tests/src/python/test_qgsserver_wms.py b/tests/src/python/test_qgsserver_wms.py
index b4598c95f34..687184c1abb 100644
--- a/tests/src/python/test_qgsserver_wms.py
+++ b/tests/src/python/test_qgsserver_wms.py
@@ -32,6 +32,7 @@ from qgis.PyQt.QtCore import QSize
 import osgeo.gdal  # NOQA
 
 from test_qgsserver import QgsServerTestBase
+from qgis.core import QgsProject
 
 # Strip path and content length because path may vary
 RE_STRIP_UNCHECKABLE = b'MAP=[^"]+|Content-Length: \d+'
@@ -196,6 +197,31 @@ class TestQgsServerWMS(QgsServerTestBase):
                                  '',
                                  'getschemaextension')
 
+    def wms_request_compare_project(self, request, extra=None, reference_file=None):
+        projectPath = self.testdata_path + "test_project.qgs"
+        assert os.path.exists(projectPath), "Project file not found: " + projectPath
+
+        project = QgsProject()
+        project.read(projectPath)
+
+        query_string = 'https://www.qgis.org/?SERVICE=WMS&VERSION=1.3&REQUEST=%s' % (request)
+        if extra is not None:
+            query_string += extra
+        header, body = self._execute_request_project(query_string, project)
+        response = header + body
+        reference_path = self.testdata_path + (request.lower() if not reference_file else reference_file) + '.txt'
+        self.store_reference(reference_path, response)
+        f = open(reference_path, 'rb')
+        expected = f.read()
+        f.close()
+        response = re.sub(RE_STRIP_UNCHECKABLE, b'*****', response)
+        expected = re.sub(RE_STRIP_UNCHECKABLE, b'*****', expected)
+
+        self.assertXMLEqual(response, expected, msg="request %s failed.\nQuery: %s\nExpected file: %s\nResponse:\n%s" % (query_string, request, reference_path, response.decode('utf-8')))
+
+    def test_wms_getcapabilities_project(self):
+        self.wms_request_compare_project('GetCapabilities')
+
     def wms_inspire_request_compare(self, request):
         """WMS INSPIRE tests"""
         project = self.testdata_path + "test_project_inspire.qgs"