diff --git a/testing/marionette/driver/marionette_driver/marionette.py b/testing/marionette/driver/marionette_driver/marionette.py
index f2c591ae5e17..436b89e12656 100644
--- a/testing/marionette/driver/marionette_driver/marionette.py
+++ b/testing/marionette/driver/marionette_driver/marionette.py
@@ -677,8 +677,7 @@ class Marionette(object):
                                                  timeout=timeout)
 
     @do_crash_check
-    def _send_message(self, command, response_key="ok", ignore_response=False,
-                      **kwargs):
+    def _send_message(self, command, response_key="ok", **kwargs):
         if not self.session_id and command != "newSession":
             raise errors.MarionetteException("Please start a session")
 
@@ -689,7 +688,7 @@ class Marionette(object):
             message["parameters"] = kwargs
 
         try:
-            response = self.client.send(message, ignore_response=ignore_response)
+            response = self.client.send(message)
         except socket.timeout:
             self.session = None
             self.window = None
@@ -909,7 +908,7 @@ class Marionette(object):
                 "eForceQuit",
                 "eRestart",
             ]
-            self._send_message('quitApplication', flags=restart_flags, ignore_response=True)
+            self._send_message('quitApplication', flags=restart_flags)
             self.client.close()
         else:
             self.delete_session()
diff --git a/testing/marionette/marionette-server.js b/testing/marionette/marionette-server.js
index c597011289e4..255303f04f7f 100644
--- a/testing/marionette/marionette-server.js
+++ b/testing/marionette/marionette-server.js
@@ -189,6 +189,7 @@ function MarionetteServerConnection(aPrefix, aTransport, aServer)
 
   this.observing = null;
   this._browserIds = new WeakMap();
+  this.quitFlags = null;
 }
 
 MarionetteServerConnection.prototype = {
@@ -228,6 +229,12 @@ MarionetteServerConnection.prototype = {
   onClosed: function MSC_onClosed(aStatus) {
     this.server._connectionClosed(this);
     this.sessionTearDown();
+
+    if (this.quitFlags !== null) {
+      let flags = this.quitFlags;
+      this.quitFlags = null;
+      Services.startup.quit(flags);
+    }
   },
 
   /**
@@ -2637,7 +2644,7 @@ MarionetteServerConnection.prototype = {
    * current session.
    */
   quitApplication: function MDA_quitApplication (aRequest) {
-    let command_id = this.getCommandId();
+    let command_id = this.command_id = this.getCommandId();
     if (appName != "Firefox") {
       this.sendError("In app initiated quit only supported on Firefox", 500, null, command_id);
     }
@@ -2648,8 +2655,13 @@ MarionetteServerConnection.prototype = {
       flags |= Ci.nsIAppStartup[k];
     }
 
-    this.sessionTearDown();
-    Services.startup.quit(flags);
+    // Close the listener so we can't re-connect until after the restart.
+    this.server.closeListener();
+    this.quitFlags = flags;
+
+    // This notifies the client it's safe to begin attempting to reconnect.
+    // The actual quit will happen when the current socket connection is closed.
+    this.sendOk(command_id);
   },
 
   /**
diff --git a/testing/marionette/transport/marionette_transport/transport.py b/testing/marionette/transport/marionette_transport/transport.py
index be6723583a1e..a72c0cb61c49 100644
--- a/testing/marionette/transport/marionette_transport/transport.py
+++ b/testing/marionette/transport/marionette_transport/transport.py
@@ -80,10 +80,8 @@ class MarionetteTransport(object):
         response = self.send({'to': 'root', 'name': 'getMarionetteID'})
         self.actor = response['id']
 
-    def send(self, msg, ignore_response=False):
+    def send(self, msg):
         """ Send a message on the socket, prepending it with len(msg) + ':'.
-        The ignore_response parameter indicates no response is expected from
-        the remote end, for instance when the client requests a quit.
         """
         if not self.sock:
             self.connect()
@@ -102,10 +100,7 @@ class MarionetteTransport(object):
                 else:
                     raise e
 
-        if not ignore_response:
-            response = self.receive()
-        else:
-            response = {'ok': True}
+        response = self.receive()
         return response
 
     def close(self):