diff --git a/.changeset/proud-candles-mix.md b/.changeset/proud-candles-mix.md
new file mode 100644
index 00000000000..8cfc63e8b11
--- /dev/null
+++ b/.changeset/proud-candles-mix.md
@@ -0,0 +1,5 @@
+---
+"@primer/react": patch
+---
+
+`UnderlineNav`: Fix icon flickering on some screen sizes before initial render/hydration
diff --git a/packages/react/src/UnderlineNav/UnderlineNav.module.css b/packages/react/src/UnderlineNav/UnderlineNav.module.css
index 329bb9e0897..7612548b008 100644
--- a/packages/react/src/UnderlineNav/UnderlineNav.module.css
+++ b/packages/react/src/UnderlineNav/UnderlineNav.module.css
@@ -2,15 +2,13 @@
   /* Progressive enhancement: Detect overflow using scroll-based animations.
   The idiomatic way would be a scroll-state container query but browser support
   is slightly better for animations. */
-  animation: detect-overflow linear;
-  animation-timeline: scroll(self block);
+  animation:
+    detect-overflow linear,
+    delay-visibility forwards 0ms 5ms;
+  animation-timeline: scroll(self block), auto;
 
   --UnderlineNav_moreButton-visibility: hidden;
-  --UnderlineNav_icons-display: inline;
-
-  &[data-hide-icons='true'] {
-    --UnderlineNav_icons-display: none;
-  }
+  --UnderlineNav_hide-icons-play-state: paused;
 
   &[data-has-overflow='true'] {
     --UnderlineNav_moreButton-visibility: visible;
@@ -21,12 +19,45 @@
   0%,
   100% {
     --UnderlineNav_moreButton-visibility: visible;
-    --UnderlineNav_icons-display: none;
+    --UnderlineNav_hide-icons-play-state: running;
   }
 }
 
 .ItemsList [data-component='icon'] {
-  display: var(--UnderlineNav_icons-display);
+  /* Unlike the more button, the icons are removed from the layout when hidden. This can cause the container to no
+  longer overflow, which would cause a flickering loop if we just drove the visibility directly from the scroll state.
+  So instead we drive an animation that can only play forwards so the icons stay hidden for the life of the page, even
+  if the container is no longer overflowing. We can't just make the scroll-driven animation itself play forwards,
+  because scroll-driven animations are conditionally applied and revert when not scrollable. */
+  animation-name: hide-icons;
+  animation-fill-mode: forwards;
+  animation-timing-function: linear;
+  animation-play-state: var(--UnderlineNav_hide-icons-play-state);
+  animation-duration: 0.1ms; /* must be greater than 0 */
+}
+
+/* Slow devices will still flicker on initial paint as we figure out if we have room to render icons or not,
+so we delay the tabs visibility by a very short time to allow things to settle. */
+@keyframes delay-visibility {
+  0%,
+  99.9% {
+    visibility: hidden;
+  }
+
+  100% {
+    visibility: visible;
+  }
+}
+
+@keyframes hide-icons {
+  0% {
+    display: inline;
+  }
+
+  0.1%,
+  100% {
+    display: none;
+  }
 }
 
 .MoreButtonContainer {
diff --git a/packages/react/src/UnderlineNav/UnderlineNav.tsx b/packages/react/src/UnderlineNav/UnderlineNav.tsx
index 5a9507cd890..a0c50f07a92 100644
--- a/packages/react/src/UnderlineNav/UnderlineNav.tsx
+++ b/packages/react/src/UnderlineNav/UnderlineNav.tsx
@@ -95,9 +95,8 @@ export const UnderlineNav = forwardRef(
           ref={navRef}
           data-variant={variant}
           data-overflow-mode="wrap"
-          // Force icons to stay hidden, avoiding flickering as icons create/remove overflow
+          // Ensure icons are hidden and button is shown on browsers that don't support scroll-driven animations
           data-hide-icons={hasEverOverflowed ? 'true' : undefined}
-          // Ensure button is shown (after initial render) on browsers that don't support scroll-driven animations
           data-has-overflow={isOverflowing ? 'true' : undefined}
         >
           <UnderlineItemList ref={listRef} role="list" className={classes.ItemsList}>
@@ -115,7 +114,7 @@ export const UnderlineNav = forwardRef(
                 variant="invisible"
                 data-component="overflow-menu-button"
                 data-current={overflowingCurrentItem ? 'true' : undefined}
-                aria-label={overflowingCurrentItem ? `More items, including current item` : undefined}
+                aria-label={overflowingCurrentItem ? 'More items, including current item' : undefined}
               >
                 <span>
                   More<VisuallyHidden as="span"> items</VisuallyHidden>
diff --git a/packages/react/src/internal/components/UnderlineTabbedInterface.module.css b/packages/react/src/internal/components/UnderlineTabbedInterface.module.css
index d1852babf0c..2ee18447239 100644
--- a/packages/react/src/internal/components/UnderlineTabbedInterface.module.css
+++ b/packages/react/src/internal/components/UnderlineTabbedInterface.module.css
@@ -29,7 +29,7 @@
 
     .UnderlineItemList {
       flex-wrap: wrap;
-      overflow: hidden;
+      flex: 1;
     }
   }
 }