--- a/browser/base/content/browser.xul
+++ b/browser/base/content/browser.xul
@@ -626,16 +626,17 @@
              aria-label="&navbarCmd.label;"
              fullscreentoolbar="true" mode="icons" customizable="true"
              iconsize="small"
              defaultset="urlbar-container,search-container,webrtc-status-button,bookmarks-menu-button,downloads-button,home-button,social-share-button,social-toolbar-item"
              customizationtarget="nav-bar-customization-target"
              overflowable="true"
              overflowbutton="nav-bar-overflow-button"
              overflowtarget="widget-overflow-list"
+             overflowpanel="widget-overflow"
              context="toolbar-context-menu">
 
       <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"
                      class="chromeclass-location" overflows="false">
           <toolbarbutton id="back-button" class="toolbarbutton-1 chromeclass-toolbar-additional"

--- a/browser/components/customizableui/src/CustomizableUI.jsm
+++ b/browser/components/customizableui/src/CustomizableUI.jsm
@@ -3450,17 +3450,22 @@ function OverflowableToolbar(aToolbarNod
 
   this._toolbar.setAttribute("overflowable", "true");
   let doc = this._toolbar.ownerDocument;
   this._target = this._toolbar.customizationTarget;
   this._list = doc.getElementById(this._toolbar.getAttribute("overflowtarget"));
   this._list.toolbox = this._toolbar.toolbox;
   this._list.customizationTarget = this._list;
 
-  Services.obs.addObserver(this, "browser-delayed-startup-finished", false);
+  let window = this._toolbar.ownerDocument.defaultView;
+  if (window.gBrowserInit.delayedStartupFinished) {
+    this.init();
+  } else {
+    Services.obs.addObserver(this, "browser-delayed-startup-finished", false);
+  }
 }
 
 OverflowableToolbar.prototype = {
   initialized: false,
   _forceOnOverflow: false,
 
   observe: function(aSubject, aTopic, aData) {
     if (aTopic == "browser-delayed-startup-finished" &&
@@ -3476,17 +3481,18 @@ OverflowableToolbar.prototype = {
     window.addEventListener("resize", this);
     window.gNavToolbox.addEventListener("customizationstarting", this);
     window.gNavToolbox.addEventListener("aftercustomization", this);
 
     let chevronId = this._toolbar.getAttribute("overflowbutton");
     this._chevron = doc.getElementById(chevronId);
     this._chevron.addEventListener("command", this);
 
-    this._panel = doc.getElementById("widget-overflow");
+    let panelId = this._toolbar.getAttribute("overflowpanel");
+    this._panel = doc.getElementById(panelId);
     this._panel.addEventListener("popuphiding", this);
     CustomizableUIInternal.addPanelCloseListeners(this._panel);
 
     CustomizableUI.addListener(this);
 
     // The 'overflow' event may have been fired before init was called.
     if (this._toolbar.overflowedDuringConstruction) {
       this.onOverflow(this._toolbar.overflowedDuringConstruction);

--- a/browser/components/customizableui/test/browser.ini
+++ b/browser/components/customizableui/test/browser.ini
@@ -69,10 +69,11 @@ skip-if = os == "linux"
 [browser_968565_insert_before_hidden_items.js]
 [browser_969427_recreate_destroyed_widget_after_reset.js]
 [browser_969661_character_encoding_navbar_disabled.js]
 [browser_970511_undo_restore_default.js]
 [browser_972267_customizationchange_events.js]
 [browser_973932_addonbar_currentset.js]
 [browser_975719_customtoolbars_behaviour.js]
 [browser_978084_dragEnd_after_move.js]
+[browser_980155_add_overflow_toolbar.js]
 [browser_981418-widget-onbeforecreated-handler.js]
 [browser_panel_toggle.js]

new file mode 100644
--- /dev/null
+++ b/browser/components/customizableui/test/browser_980155_add_overflow_toolbar.js
@@ -0,0 +1,51 @@
+/* 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/. */
+
+"use strict";
+
+const kToolbarName = "test-new-overflowable-toolbar";
+const kTestWidgetPrefix = "test-widget-for-overflowable-toolbar-";
+
+add_task(function addOverflowingToolbar() {
+  let originalWindowWidth = window.outerWidth;
+
+  let widgetIds = [];
+  for (let i = 0; i < 10; i++) {
+    let id = kTestWidgetPrefix + i;
+    widgetIds.push(id);
+    let spec = {id: id, type: "button", removable: true, label: "test", tooltiptext: "" + i};
+    CustomizableUI.createWidget(spec);
+  }
+
+  let toolbarNode = createOverflowableToolbarWithPlacements(kToolbarName, widgetIds);
+  assertAreaPlacements(kToolbarName, widgetIds);
+
+  for (let id of widgetIds) {
+    document.getElementById(id).style.minWidth = "200px";
+  }
+
+  isnot(toolbarNode.overflowable, null, "Toolbar should have overflowable controller");
+  isnot(toolbarNode.customizationTarget, null, "Toolbar should have customization target");
+  isnot(toolbarNode.customizationTarget, toolbarNode, "Customization target should not be toolbar node");
+
+  let oldChildCount = toolbarNode.customizationTarget.childElementCount;
+  let overflowableList = document.getElementById(kToolbarName + "-overflow-list");
+  let oldOverflowCount = overflowableList.childElementCount;
+
+  isnot(oldChildCount, 0, "Toolbar should have non-overflowing widgets");
+
+  window.resizeTo(400, window.outerHeight);
+  yield waitForCondition(() => toolbarNode.hasAttribute("overflowing"));
+  ok(toolbarNode.hasAttribute("overflowing"), "Should have an overflowing toolbar.");
+  ok(toolbarNode.customizationTarget.childElementCount < oldChildCount, "Should have fewer children.");
+  ok(overflowableList.childElementCount > oldOverflowCount, "Should have more overflowed widgets.");
+
+  window.resizeTo(originalWindowWidth, window.outerHeight);
+});
+
+
+add_task(function asyncCleanup() {
+  removeCustomToolbars();
+  yield resetCustomization();
+});

--- a/browser/components/customizableui/test/head.js
+++ b/browser/components/customizableui/test/head.js
@@ -40,21 +40,67 @@ function createToolbarWithPlacements(id,
   CustomizableUI.registerArea(id, {
     type: CustomizableUI.TYPE_TOOLBAR,
     defaultPlacements: placements
   });
   gNavToolbox.appendChild(tb);
   return tb;
 }
 
+function createOverflowableToolbarWithPlacements(id, placements) {
+  gAddedToolbars.add(id);
+
+  let tb = document.createElementNS(kNSXUL, "toolbar");
+  tb.id = id;
+  tb.setAttribute("customizationtarget", id + "-target");
+
+  let customizationtarget = document.createElementNS(kNSXUL, "hbox");
+  customizationtarget.id = id + "-target";
+  customizationtarget.setAttribute("flex", "1");
+  tb.appendChild(customizationtarget);
+
+  let overflowPanel = document.createElementNS(kNSXUL, "panel");
+  overflowPanel.id = id + "-overflow";
+  document.getElementById("mainPopupSet").appendChild(overflowPanel);
+
+  let overflowList = document.createElementNS(kNSXUL, "vbox");
+  overflowList.id = id + "-overflow-list";
+  overflowPanel.appendChild(overflowList);
+
+  let chevron = document.createElementNS(kNSXUL, "toolbarbutton");
+  chevron.id = id + "-chevron";
+  tb.appendChild(chevron);
+
+  CustomizableUI.registerArea(id, {
+    type: CustomizableUI.TYPE_TOOLBAR,
+    defaultPlacements: placements,
+    overflowable: true,
+  });
+
+  tb.setAttribute("customizable", "true");
+  tb.setAttribute("overflowable", "true");
+  tb.setAttribute("overflowpanel", overflowPanel.id);
+  tb.setAttribute("overflowtarget", overflowList.id);
+  tb.setAttribute("overflowbutton", chevron.id);
+
+  gNavToolbox.appendChild(tb);
+  return tb;
+}
+
 function removeCustomToolbars() {
   CustomizableUI.reset();
   for (let toolbarId of gAddedToolbars) {
     CustomizableUI.unregisterArea(toolbarId, true);
-    document.getElementById(toolbarId).remove();
+    let tb = document.getElementById(toolbarId);
+    if (tb.hasAttribute("overflowpanel")) {
+      let panel = document.getElementById(tb.getAttribute("overflowpanel"));
+      if (panel)
+        panel.remove();
+    }
+    tb.remove();
   }
   gAddedToolbars.clear();
 }
 
 function getToolboxCustomToolbarId(toolbarName) {
   return "__customToolbar_" + toolbarName.replace(" ", "_");
 }