--- a/testing/marionette/driver.js
+++ b/testing/marionette/driver.js
@@ -125,17 +125,17 @@ this.GeckoDriver = function(appId, serve
   this.appId = appId;
   this._server = server;
 
   this.sessionID = null;
   this.wins = new browser.Windows();
   this.browsers = {};
   // points to current browser
   this.curBrowser = null;
-  // topmost chrome frame
+  // top-most chrome window
   this.mainFrame = null;
   // chrome iframe that currently has focus
   this.curFrame = null;
   this.currentFrameElement = null;
   this.observing = null;
   this._browserIds = new WeakMap();
 
   // Use content context by default
@@ -2829,25 +2829,19 @@ GeckoDriver.prototype.deleteSession = fu
         win.messageManager.removeDelayedFrameScript(FRAME_SCRIPT);
       } else {
         logger.error(
             `Could not remove listener from page ${win.location.href}`);
       }
     }
   }
 
-  // reset frame to the top-most frame
+  // reset frame to the top-most frame, and clear reference to chrome window
   this.curFrame = null;
-  if (this.mainFrame) {
-    try {
-      this.mainFrame.focus();
-    } catch (e) {
-      this.mainFrame = null;
-    }
-  }
+  this.mainFrame = null;
 
   if (this.observing !== null) {
     for (let topic in this.observing) {
       Services.obs.removeObserver(this.observing[topic], topic);
     }
     this.observing = null;
   }
 

--- a/testing/marionette/server.js
+++ b/testing/marionette/server.js
@@ -288,16 +288,25 @@ class TCPConnection {
     if (typeof fn == "undefined") {
       throw new UnknownCommandError(cmd.name);
     }
 
     if (!["newSession", "WebDriver:NewSession"].includes(cmd.name)) {
       assert.session(this.driver);
     }
 
+    // With the focusmanager testmode enabled the currently selected
+    // chrome window of Firefox has to virtually be brought into foreground
+    // so that focus events will be fired when interacting with UI elements.
+    // This has to be done for each and every command, given that the
+    // application focus can change at any time.
+    if (this.driver.mainFrame !== null) {
+      this.driver.mainFrame.focus();
+    }
+
     let rv = await fn.bind(this.driver)(cmd);
 
     if (rv != null) {
       if (rv instanceof WebElement || typeof rv != "object") {
         resp.body = {value: rv};
       } else {
         resp.body = rv;
       }