diff --git a/src/components/selectable/selectable_list/_selectable_list.scss b/src/components/selectable/selectable_list/_selectable_list.scss
index 6e314a96eec..a48d32679e7 100644
--- a/src/components/selectable/selectable_list/_selectable_list.scss
+++ b/src/components/selectable/selectable_list/_selectable_list.scss
@@ -1,10 +1,12 @@
-// Expand height of list via flex box
 .euiSelectableList {
-  &:focus-within {
-    @include euiFocusRing;
+  // NOTE: This is currently only visible on supported browsers (all except FF)
+  // which is (unfortunately) better than always displaying the focus ring to mouse users
+  &:has(:focus-visible) {
+    @include euiFocusRing(null, $euiFocusRingSize / 2, false);
   }
 }
 
+// Expand height of list via flex box
 .euiSelectableList-fullHeight {
   flex-grow: 1;
 }
@@ -18,6 +20,11 @@
 .euiSelectableList__list {
   @include euiOverflowShadow;
   @include euiScrollBar;
+
+  &:focus,
+  & > ul:focus {
+    outline: none; // Focus outline handled by parent .euiSelectableList
+  }
 }
 
 .euiSelectableList__groupLabel {
diff --git a/src/themes/amsterdam/global_styling/mixins/_states.scss b/src/themes/amsterdam/global_styling/mixins/_states.scss
index 27698e2ab06..81279d81b98 100644
--- a/src/themes/amsterdam/global_styling/mixins/_states.scss
+++ b/src/themes/amsterdam/global_styling/mixins/_states.scss
@@ -3,22 +3,31 @@
 // This re-uses the same faux focus ring mixin, but adjusts the outline instead
 // @param {size} Old param from default theme that won't be used, so it should always be `null`
 // @param {offset} Accepts a specific number or 'inner' or 'outer' to adjust outline position
-@mixin euiFocusRing($size: null, $offset: false) {
+// @param {includeFocusVisible} Allows turning off :not:focus-visible selector (which can interfere with some manual usages)
+@mixin euiFocusRing($size: null, $offset: false, $focusVisibleSelectors: true) {
   // Safari & Firefox
   outline: $euiFocusRingSize solid currentColor;
 
-  // Chrome
-  &:focus-visible {
-    outline-style: auto;
-  }
+  @if ($focusVisibleSelectors) {
+    // Chrome
+    &:focus-visible {
+      outline-style: auto;
+    }
 
-  &:not(:focus-visible) {
-    outline: none;
+    &:not(:focus-visible) {
+      outline: none;
+    }
+  } @else {
+    outline-style: auto;
   }
 
   // Adjusting position with offset
   @if (type-of($offset) == number) {
-    outline-offset: #{$offset}px;
+    @if (unitless($offset)) {
+      outline-offset: #{$offset}px;
+    } @else {
+      outline-offset: #{$offset};
+    }
   } @else if ($offset == 'inner') {
     outline-offset: -$euiFocusRingSize;
   } @else if ($offset == 'outer') {
diff --git a/upcoming_changelogs/6637.md b/upcoming_changelogs/6637.md
new file mode 100644
index 00000000000..8698eac8be7
--- /dev/null
+++ b/upcoming_changelogs/6637.md
@@ -0,0 +1,3 @@
+**Bug fixes**
+
+- Fixed visual listbox focus ring bug on non-searchable `EuiSelectable`s