diff --git a/ycmd/completers/language_server/language_server_completer.py b/ycmd/completers/language_server/language_server_completer.py
index a2796e81ce..b5fd6ee182 100644
--- a/ycmd/completers/language_server/language_server_completer.py
+++ b/ycmd/completers/language_server/language_server_completer.py
@@ -1005,7 +1005,8 @@ def __init__( self, user_options, connection_type = 'stdio' ):
     self._on_file_ready_to_parse_handlers = []
     self.RegisterOnFileReadyToParse(
       lambda self, request_data:
-        self._UpdateServerWithFileContents( request_data )
+        self._UpdateServerWithFileContents( request_data ),
+      True # once
     )
 
     self._signature_help_disabled = user_options[ 'disable_signature_help' ]
@@ -1898,6 +1899,12 @@ def OnFileReadyToParse( self, request_data ):
     if not self.ServerIsHealthy():
       return
 
+    def ClearOneshotHandlers():
+      self._on_file_ready_to_parse_handlers = [
+        ( handler, once ) for handler, once
+        in self._on_file_ready_to_parse_handlers if not once
+      ]
+
     # If we haven't finished initializing yet, we need to queue up all functions
     # registered on the FileReadyToParse event and in particular
     # _UpdateServerWithFileContents in reverse order of registration. This
@@ -1905,13 +1912,17 @@ def OnFileReadyToParse( self, request_data ):
     # messages. This is important because server start up can be quite slow and
     # we must not block the user, while we must keep the server synchronized.
     if not self._initialize_event.is_set():
-      for handler in reversed( self._on_file_ready_to_parse_handlers ):
+      for handler, _ in reversed( self._on_file_ready_to_parse_handlers ):
         self._OnInitializeComplete( partial( handler,
                                              request_data = request_data ) )
+      ClearOneshotHandlers()
       return
 
-    for handler in reversed( self._on_file_ready_to_parse_handlers ):
+    for handler, _ in reversed( self._on_file_ready_to_parse_handlers ):
       handler( self, request_data )
+    ClearOneshotHandlers()
+
+    self._UpdateServerWithFileContents( request_data )
 
     # Return the latest diagnostics that we have received.
     #
@@ -2480,8 +2491,8 @@ def _OnInitializeComplete( self, handler ):
     self._on_initialize_complete_handlers.append( handler )
 
 
-  def RegisterOnFileReadyToParse( self, handler ):
-    self._on_file_ready_to_parse_handlers.append( handler )
+  def RegisterOnFileReadyToParse( self, handler, once=False ):
+    self._on_file_ready_to_parse_handlers.append( ( handler, once ) )
 
 
   def GetHoverResponse( self, request_data ):
diff --git a/ycmd/tests/rust/__init__.py b/ycmd/tests/rust/__init__.py
index 4c604f7837..16df6fed84 100644
--- a/ycmd/tests/rust/__init__.py
+++ b/ycmd/tests/rust/__init__.py
@@ -44,10 +44,11 @@ def tearDownModule():
 
 def StartRustCompleterServerInDirectory( app, directory ):
   app.post_json( '/event_notification',
-                 BuildRequest(
-                   filepath = os.path.join( directory, 'src', 'main.rs' ),
-                   event_name = 'FileReadyToParse',
-                   filetype = 'rust' ) )
+                 BuildRequest( filepath = os.path.join( directory,
+                                                        'src',
+                                                        'main.rs' ),
+                               event_name = 'FileReadyToParse',
+                               filetype = 'rust' ) )
   WaitUntilCompleterServerReady( app, 'rust' )
 
 
diff --git a/ycmd/tests/test_utils.py b/ycmd/tests/test_utils.py
index e7b725db4a..55b091b5d2 100644
--- a/ycmd/tests/test_utils.py
+++ b/ycmd/tests/test_utils.py
@@ -16,6 +16,7 @@
 # along with ycmd.  If not, see <http://www.gnu.org/licenses/>.
 
 
+from ycmd.utils import ReadFile
 from hamcrest import ( assert_that,
                        contains_exactly,
                        contains_string,
@@ -76,9 +77,22 @@
 } )
 
 
+def GetTestFileContents( filename ):
+  try:
+    return ReadFile( filename )
+  except IOError:
+    return ''
+
+
 def BuildRequest( **kwargs ):
   filepath = kwargs[ 'filepath' ] if 'filepath' in kwargs else '/foo'
-  contents = kwargs[ 'contents' ] if 'contents' in kwargs else ''
+  contents = (
+    kwargs[ 'contents' ]
+    if 'contents' in kwargs
+    else GetTestFileContents( filepath )
+      if 'filepath' in kwargs
+      else ''
+  )
   filetype = kwargs[ 'filetype' ] if 'filetype' in kwargs else 'foo'
   filetypes = kwargs[ 'filetypes' ] if 'filetypes' in kwargs else [ filetype ]