--- a/testing/marionette/components/marionette.js
+++ b/testing/marionette/components/marionette.js
@@ -14,16 +14,17 @@ ChromeUtils.defineModuleGetter(this, "Lo
 ChromeUtils.defineModuleGetter(this, "Preferences",
     "resource://gre/modules/Preferences.jsm");
 XPCOMUtils.defineLazyGetter(this, "log", () => {
   let log = Log.repository.getLogger("Marionette");
   log.addAppender(new Log.DumpAppender());
   return log;
 });
 
+const PREF_ENABLED = "marionette.enabled";
 const PREF_PORT = "marionette.port";
 const PREF_PORT_FALLBACK = "marionette.defaultPrefs.port";
 const PREF_LOG_LEVEL = "marionette.log.level";
 const PREF_LOG_LEVEL_FALLBACK = "marionette.logging";
 
 const DEFAULT_LOG_LEVEL = "info";
 const NOTIFY_RUNNING = "remote-active";
 
@@ -146,26 +147,44 @@ class MarionetteComponent {
 
     // indicates that all pending window checks have been completed
     // and that we are ready to start the Marionette server
     this.finalUIStartup = false;
 
     log.level = prefs.logLevel;
 
     this.enabled = env.exists(ENV_ENABLED);
+
+    Services.prefs.addObserver(PREF_ENABLED, this);
   }
 
   get running() {
     return this.server && this.server.alive;
   }
 
+  set enabled(value) {
+    Services.prefs.setBoolPref(PREF_ENABLED, value);
+  }
+
+  get enabled() {
+    return Services.prefs.getBoolPref(PREF_ENABLED);
+  }
+
   observe(subject, topic) {
     log.debug(`Received observer notification ${topic}`);
 
     switch (topic) {
+      case "nsPref:changed":
+        if (Services.prefs.getBoolPref(PREF_ENABLED)) {
+          this.init();
+        } else {
+          this.uninit();
+        }
+        break;
+
       case "profile-after-change":
         Services.obs.addObserver(this, "command-line-startup");
         Services.obs.addObserver(this, "sessionstore-windows-restored");
 
         prefs.readFromEnvironment(ENV_PRESERVE_PREFS);
         break;
 
       // In safe mode the command line handlers are getting parsed after the
@@ -282,16 +301,17 @@ class MarionetteComponent {
       Services.obs.notifyObservers(this, NOTIFY_RUNNING);
     }
   }
 
   get QueryInterface() {
     return XPCOMUtils.generateQI([
       Ci.nsICommandLineHandler,
       Ci.nsIMarionette,
+      Ci.nsIObserver,
     ]);
   }
 }
 
 const MarionetteFactory = {
   createInstance(outer, iid) {
     if (outer) {
       throw Cr.NS_ERROR_NO_AGGREGATION;

--- a/testing/marionette/prefs/marionette.js
+++ b/testing/marionette/prefs/marionette.js
@@ -1,26 +1,25 @@
 /* This Source Code Form is subject to the terms of the Mozilla Public
  * License, v. 2.0. If a copy of the MPL was not distributed with this file,
  * You can obtain one at http://mozilla.org/MPL/2.0/. */
 
 /* global pref */
 
 // Marionette is the remote protocol that lets OOP programs communicate
 // with, instrument, and control Gecko.
-//
-// It is included in Firefox, but not enabled by default unless the
-// -marionette flag is passed.
+
+// Controls whether the Marionette component is enabled.
+pref("marionette.enabled", false);
 
 // Delay server startup until a modal dialogue has been clicked to
 // allow time for user to set breakpoints in Browser Toolbox.
 pref("marionette.debugging.clicktostart", false);
 
 // Marionette logging verbosity.  Allowed values are "fatal", "error",
 // "warn", "info", "config", "debug", and "trace".
 pref("marionette.log.level", "info");
 
 // Port to start Marionette server on.
 pref("marionette.port", 2828);
 
-// Sets preferences recommended when using Firefox in automation with
-// Marionette.
+// Sets recommended automation preferences when Marionette is started.
 pref("marionette.prefs.recommended", true);