--- a/browser/base/content/browser.css
+++ b/browser/base/content/browser.css
@@ -1245,29 +1245,29 @@ toolbarpaletteitem[place="palette"] > #d
 }
 
 #customization-panelHolder {
   padding-top: 10px;
   padding-bottom: 10px;
 }
 
 #customization-panelHolder > #widget-overflow-fixed-list {
-  flex: 0 1 auto; /* Size to content, but allow ourselves to shrink */
+  flex: 1 1 auto; /* Grow within the available space, and allow ourselves to shrink */
   display: flex;
   flex-direction: column;
   overflow-y: auto;
   overflow-x: hidden;
 }
 
 #customization-panelWrapper,
 #customization-panelWrapper > .panel-arrowcontent,
 #customization-panelHolder {
   flex-direction: column;
   display: flex;
-  min-height: 0;
+  min-height: calc(174px + 8em);
 }
 
 #customization-panelWrapper {
   flex: 1 1 auto;
   height: 0; /* Don't let my contents affect ancestors' content-based sizing */
   align-items: end; /* align to the end on the cross-axis (affects arrow) */
 }
 

--- a/browser/themes/shared/customizableui/customizeMode.inc.css
+++ b/browser/themes/shared/customizableui/customizeMode.inc.css
@@ -506,17 +506,16 @@ toolbarpaletteitem[place=toolbar] > tool
   font-size: 1.3em;
   font-weight: 500;
   padding: 2px 12px;
   margin: 0;
 }
 
 #customization-panelHolder > #widget-overflow-fixed-list {
   padding-top: 10px;
-  min-height: 225px;
 }
 
 /**
  * We create a ::before pseudoelement that contains a background image to show the
  * drop dragon. This element fades in and out depending on whether the containing
  * panel list is empty and unhovered, or not.
  */
 #customization-panelHolder > #widget-overflow-fixed-list:not(:empty) {