diff --git a/browser/extensions/formautofill/FormAutofillContent.jsm b/browser/extensions/formautofill/FormAutofillContent.jsm
index f5ea0cce7a55..740b8906a5b9 100644
--- a/browser/extensions/formautofill/FormAutofillContent.jsm
+++ b/browser/extensions/formautofill/FormAutofillContent.jsm
@@ -587,14 +587,8 @@ var FormAutofillContent = {
       this._activeItems = {};
       return;
     }
-    let handler = this._getFormHandler(element);
-    if (handler) {
-      handler.focusedInput = element;
-    }
     this._activeItems = {
-      handler,
       elementWeakRef: Cu.getWeakReference(element),
-      section: handler ? handler.activeSection : null,
       fieldDetail: null,
     };
   },
@@ -605,11 +599,25 @@ var FormAutofillContent = {
   },
 
   get activeHandler() {
-    return this._activeItems.handler;
+    const activeInput = this.activeInput;
+    if (!activeInput) {
+      return null;
+    }
+
+    // XXX: We are recomputing the activeHandler every time to avoid keeping a
+    // reference on the active element. This might be called quite frequently
+    // so if _getFormHandler/findRootForField become more costly, we should
+    // look into caching this result (eg by adding a weakmap).
+    let handler = this._getFormHandler(activeInput);
+    if (handler) {
+      handler.focusedInput = activeInput;
+    }
+    return handler;
   },
 
   get activeSection() {
-    return this._activeItems.section;
+    let formHandler = this.activeHandler;
+    return formHandler ? formHandler.activeSection : null;
   },
 
   /**
diff --git a/browser/extensions/formautofill/content/FormAutofillFrameScript.js b/browser/extensions/formautofill/content/FormAutofillFrameScript.js
index d37fd573365b..88fe15b5a65e 100644
--- a/browser/extensions/formautofill/content/FormAutofillFrameScript.js
+++ b/browser/extensions/formautofill/content/FormAutofillFrameScript.js
@@ -78,10 +78,6 @@ var FormAutofillFrameScript = {
         this.onFocusIn(evt);
         break;
       }
-      case "focusout": {
-        this.onFocusOut();
-        break;
-      }
       case "DOMFormBeforeSubmit": {
         this.onDOMFormBeforeSubmit(evt);
         break;
@@ -120,12 +116,6 @@ var FormAutofillFrameScript = {
     this._doIdentifyAutofillFields();
   },
 
-  onFocusOut() {
-    // Update active input on blur to release references on the previously
-    // focused element in FormAutofillContent.
-    FormAutofillContent.updateActiveInput();
-  },
-
   /**
    * Handle the DOMFormBeforeSubmit event.
    * @param {Event} evt
diff --git a/browser/extensions/formautofill/test/browser/focus-leak/browser_iframe_typecontent_input_focus.js b/browser/extensions/formautofill/test/browser/focus-leak/browser_iframe_typecontent_input_focus.js
index 3091dc12566c..74b25994be62 100644
--- a/browser/extensions/formautofill/test/browser/focus-leak/browser_iframe_typecontent_input_focus.js
+++ b/browser/extensions/formautofill/test/browser/focus-leak/browser_iframe_typecontent_input_focus.js
@@ -50,6 +50,6 @@ add_task(async function() {
     "The .focusme input is the active element"
   );
 
-  // Stop the test without blurring the input, the cleanup should still prevent
-  // leaks in the test.
+  info("Remove the focused input");
+  focusMeInput.remove();
 });