diff --git a/browser/base/content/browser.xul b/browser/base/content/browser.xul
index 0b033b3db0a..fb59101988c 100644
--- a/browser/base/content/browser.xul
+++ b/browser/base/content/browser.xul
@@ -628,7 +628,7 @@
              overflowtarget="widget-overflow-list"
              context="toolbar-context-menu">
 
-      <hbox id="nav-bar-customization-target" class="customization-target" flex="1">
+      <hbox id="nav-bar-customization-target" flex="1">
         <toolbaritem id="urlbar-container" flex="400" persist="width"
                      forwarddisabled="true" title="&locationItem.title;" removable="false"
                      cui-areatype="toolbar"
diff --git a/browser/components/customizableui/src/CustomizableUI.jsm b/browser/components/customizableui/src/CustomizableUI.jsm
index 978f594881b..d2e974195b1 100644
--- a/browser/components/customizableui/src/CustomizableUI.jsm
+++ b/browser/components/customizableui/src/CustomizableUI.jsm
@@ -794,6 +794,10 @@ let CustomizableUIInternal = {
     }
 
     gBuildAreas.get(aArea).add(aNode);
+
+    // Give a class to all customize targets to be used for styling in Customize Mode
+    let customizableNode = this.getCustomizeTargetForArea(aArea, window);
+    customizableNode.classList.add("customization-target");
   },
 
   registerBuildWindow: function(aWindow) {
diff --git a/browser/components/customizableui/src/CustomizeMode.jsm b/browser/components/customizableui/src/CustomizeMode.jsm
index 217b079c999..9664c019e8b 100644
--- a/browser/components/customizableui/src/CustomizeMode.jsm
+++ b/browser/components/customizableui/src/CustomizeMode.jsm
@@ -1475,6 +1475,7 @@ CustomizeMode.prototype = {
       this._cancelDragActive(this._dragOverItem);
       this._dragOverItem = null;
     }
+    this._updateToolbarCustomizationOutline(this.window);
     this._showPanelCustomizationPlaceholders();
   },
 
@@ -1511,6 +1512,7 @@ CustomizeMode.prototype = {
         this._setGridDragActive(aItem, draggedItem, aValue);
       } else {
         let targetArea = this._getCustomizableParent(aItem);
+        this._updateToolbarCustomizationOutline(window, targetArea);
         let makeSpaceImmediately = false;
         if (!gDraggingInToolbars.has(targetArea.id)) {
           gDraggingInToolbars.add(targetArea.id);
@@ -1545,6 +1547,7 @@ CustomizeMode.prototype = {
     }
   },
   _cancelDragActive: function(aItem, aNextItem, aNoTransition) {
+    this._updateToolbarCustomizationOutline(aItem.ownerDocument.defaultView);
     let currentArea = this._getCustomizableParent(aItem);
     if (!currentArea) {
       return;
@@ -1771,7 +1774,36 @@ CustomizeMode.prototype = {
     while (oldPlaceholders.length) {
       contents.removeChild(oldPlaceholders[0]);
     }
-  }
+  },
+
+  /**
+   * Update toolbar customization targets during drag events to add or remove
+   * outlines to indicate that an area is customizable.
+   *
+   * @param aWindow                       The XUL window in which outlines should be updated.
+   * @param {Element} [aToolbarArea=null] The element of the customizable toolbar area to add the
+   *                                      outline to. If aToolbarArea is falsy, the outline will be
+   *                                      removed from all toolbar areas.
+   */
+  _updateToolbarCustomizationOutline: function(aWindow, aToolbarArea = null) {
+    // Remove the attribute from existing customization targets
+    for (let area of CustomizableUI.areas) {
+      if (CustomizableUI.getAreaType(area) != CustomizableUI.TYPE_TOOLBAR) {
+        continue;
+      }
+      let target = CustomizableUI.getCustomizeTargetForArea(area, aWindow);
+      target.removeAttribute("customizing-dragovertarget");
+    }
+
+    // Now set the attribute on the desired target
+    if (aToolbarArea) {
+      if (CustomizableUI.getAreaType(aToolbarArea.id) != CustomizableUI.TYPE_TOOLBAR)
+        return;
+      let target = CustomizableUI.getCustomizeTargetForArea(aToolbarArea.id, aWindow);
+      target.setAttribute("customizing-dragovertarget", true);
+    }
+  },
+
 };
 
 function __dumpDragData(aEvent, caller) {