diff --git a/webui/src/components/thread/PromptRail.tsx b/webui/src/components/thread/PromptRail.tsx
index 52e6cf6f..dbc87b34 100644
--- a/webui/src/components/thread/PromptRail.tsx
+++ b/webui/src/components/thread/PromptRail.tsx
@@ -12,7 +12,6 @@ import {
 
 interface PromptRailProps {
   bottomOffset: number;
-  contentRef: RefObject<HTMLElement>;
   messages: UIMessage[];
   scrollRef: RefObject<HTMLDivElement>;
 }
@@ -43,19 +42,9 @@ const MARKER_STACK_GAP_PX = 16;
 const RAIL_FALLBACK_HEIGHT_PX = 300;
 const MEASURE_RETRY_FRAMES = 4;
 const HOVER_MARKER_WIDTHS_PX = [28, 22, 16, 11];
-const RAIL_WIDTH_PX = 36;
-const RAIL_MIN_EDGE_GAP_PX = 12;
-const RAIL_COLUMN_GAP_PX = 20;
-const RAIL_REQUIRED_GUTTER_PX = RAIL_MIN_EDGE_GAP_PX + RAIL_WIDTH_PX + RAIL_COLUMN_GAP_PX;
-
-interface RailLayout {
-  visible: boolean;
-  left: number | null;
-}
 
 export function PromptRail({
   bottomOffset,
-  contentRef,
   messages,
   scrollRef,
 }: PromptRailProps) {
@@ -64,41 +53,12 @@ export function PromptRail({
   const [markers, setMarkers] = useState<PromptMarker[]>([]);
   const [activePromptId, setActivePromptId] = useState<string | null>(null);
   const [focusedMarkerIndex, setFocusedMarkerIndex] = useState<number | null>(null);
-  const [railLayout, setRailLayout] = useState<RailLayout>({ visible: true, left: null });
-
-  const measureRailLayout = useCallback((): RailLayout => {
-    const scrollEl = scrollRef.current;
-    const contentEl = contentRef.current;
-    if (!scrollEl || !contentEl) return { visible: true, left: null };
-
-    const scrollRect = scrollEl.getBoundingClientRect();
-    const contentRect = contentEl.getBoundingClientRect();
-    if (scrollRect.width <= 0 || contentRect.width <= 0) {
-      return { visible: true, left: null };
-    }
-
-    const leftGutter = contentRect.left - scrollRect.left;
-    if (leftGutter < RAIL_REQUIRED_GUTTER_PX) {
-      return { visible: false, left: null };
-    }
-
-    return {
-      visible: true,
-      left: Math.round(leftGutter - RAIL_WIDTH_PX - RAIL_COLUMN_GAP_PX),
-    };
-  }, [contentRef, scrollRef]);
 
   const updateMarkers = useCallback(() => {
     const scrollEl = scrollRef.current;
     const nextRailHeight = railRef.current?.clientHeight ?? 0;
-    const nextRailLayout = measureRailLayout();
-    setRailLayout((current) =>
-      current.visible === nextRailLayout.visible && current.left === nextRailLayout.left
-        ? current
-        : nextRailLayout,
-    );
 
-    if (!nextRailLayout.visible || !scrollEl || promptAnchors.length < MIN_PROMPTS_FOR_RAIL) {
+    if (!scrollEl || promptAnchors.length < MIN_PROMPTS_FOR_RAIL) {
       setMarkers([]);
       setActivePromptId(null);
       return;
@@ -115,7 +75,7 @@ export function PromptRail({
     const grouped = groupPromptMarkers(measured, nextRailHeight);
     setMarkers(distributeMarkerPositions(grouped, nextRailHeight));
     setActivePromptId(activePromptForScroll(measured, scrollEl.scrollTop));
-  }, [measureRailLayout, promptAnchors, scrollRef]);
+  }, [promptAnchors, scrollRef]);
 
   useEffect(() => {
     let frame = 0;
@@ -156,26 +116,22 @@ export function PromptRail({
     const observer = new ResizeObserver(() => updateMarkers());
     observer.observe(scrollEl);
     if (scrollEl.firstElementChild) observer.observe(scrollEl.firstElementChild);
-    if (contentRef.current) observer.observe(contentRef.current);
     return () => observer.disconnect();
-  }, [contentRef, scrollRef, updateMarkers]);
+  }, [scrollRef, updateMarkers]);
 
-  if (!railLayout.visible || markers.length === 0) return null;
+  if (markers.length === 0) return null;
 
   return (
     <div
       ref={railRef}
       aria-label="User prompt navigation"
       className={cn(
-        "group pointer-events-auto absolute left-7 top-3 z-20 hidden w-9 opacity-100 md:block",
+        "thread-prompt-rail group pointer-events-auto absolute top-3 z-20 w-9 opacity-100",
         "transition-opacity duration-200",
         "motion-safe:animate-in motion-safe:fade-in-0 motion-safe:duration-200",
       )}
       onPointerLeave={() => setFocusedMarkerIndex(null)}
-      style={{
-        bottom: Math.max(80, bottomOffset),
-        ...(railLayout.left == null ? {} : { left: railLayout.left }),
-      }}
+      style={{ bottom: Math.max(80, bottomOffset) }}
     >
       {markers.map((marker, index) => {
         const active = marker.ids.includes(activePromptId ?? "");
diff --git a/webui/src/components/thread/ThreadViewport.tsx b/webui/src/components/thread/ThreadViewport.tsx
index 48d62818..685bc066 100644
--- a/webui/src/components/thread/ThreadViewport.tsx
+++ b/webui/src/components/thread/ThreadViewport.tsx
@@ -122,7 +122,6 @@ export const ThreadViewport = forwardRef<ThreadViewportHandle, ThreadViewportPro
   const { t } = useTranslation();
   const scrollRef = useRef<HTMLDivElement>(null);
   const contentRef = useRef<HTMLDivElement>(null);
-  const messageColumnRef = useRef<HTMLDivElement>(null);
   const composerDockRef = useRef<HTMLDivElement>(null);
   const bottomRef = useRef<HTMLDivElement>(null);
   const lastConversationKeyRef = useRef<string | null>(conversationKey);
@@ -502,7 +501,7 @@ export const ThreadViewport = forwardRef<ThreadViewportHandle, ThreadViewportPro
   }, [maybeLoadEarlierFromScroll]);
 
   return (
-    <div className="relative flex min-h-0 flex-1 overflow-hidden">
+    <div className="thread-viewport relative flex min-h-0 flex-1 overflow-hidden">
       <div
         ref={scrollRef}
         className={cn(
@@ -520,11 +519,7 @@ export const ThreadViewport = forwardRef<ThreadViewportHandle, ThreadViewportPro
               data-testid="thread-message-region"
               className="flex min-h-0 flex-1 flex-col justify-start px-3 pb-4 pt-4 sm:px-4"
             >
-              <div
-                ref={messageColumnRef}
-                data-testid="thread-message-column"
-                className="mx-auto w-full max-w-[49.5rem]"
-              >
+              <div className="mx-auto w-full max-w-[49.5rem]">
                 <ThreadMessages
                   messages={visibleMessages}
                   isStreaming={isStreaming}
@@ -572,7 +567,6 @@ export const ThreadViewport = forwardRef<ThreadViewportHandle, ThreadViewportPro
         <PromptRail
           messages={visibleMessages}
           scrollRef={scrollRef}
-          contentRef={messageColumnRef}
           bottomOffset={scrollButtonBottom}
         />
       ) : null}
diff --git a/webui/src/globals.css b/webui/src/globals.css
index 64edeae5..81d2dd53 100644
--- a/webui/src/globals.css
+++ b/webui/src/globals.css
@@ -568,4 +568,30 @@
   .thread-viewport-scrollbar {
     overflow-x: hidden;
   }
+
+  .thread-viewport {
+    --thread-message-column-half: 24.75rem;
+    --thread-prompt-rail-offset: 3.5rem;
+    container-name: thread-viewport;
+    container-type: inline-size;
+  }
+
+  .thread-prompt-rail {
+    display: none;
+    left: calc(
+      50% - var(--thread-message-column-half) - var(--thread-prompt-rail-offset)
+    );
+  }
+
+  @media (min-width: 768px) {
+    .thread-prompt-rail {
+      display: block;
+    }
+  }
+
+  @container thread-viewport (max-width: 58rem) {
+    .thread-prompt-rail {
+      display: none;
+    }
+  }
 }
diff --git a/webui/src/tests/thread-viewport.test.tsx b/webui/src/tests/thread-viewport.test.tsx
index 447ae8ca..acd087d2 100644
--- a/webui/src/tests/thread-viewport.test.tsx
+++ b/webui/src/tests/thread-viewport.test.tsx
@@ -132,35 +132,9 @@ function makePromptExchangeMessages(count: number): UIMessage[] {
   ])).flat();
 }
 
-function elementRect(left: number, width: number, height = 600): DOMRect {
-  return {
-    x: left,
-    y: 0,
-    left,
-    top: 0,
-    right: left + width,
-    bottom: height,
-    width,
-    height,
-    toJSON: () => ({}),
-  } as DOMRect;
-}
-
-function stubElementRect(element: HTMLElement, left: number, width: number, height = 600) {
-  element.getBoundingClientRect = () => elementRect(left, width, height);
-}
-
-interface PromptRailLayoutStub {
-  scrollerWidth: number;
-  messageColumnLeft: number;
-  messageColumnWidth: number;
-}
-
 async function renderPromptRailViewport({
-  layout,
   scrollTo,
 }: {
-  layout?: PromptRailLayoutStub;
   scrollTo?: (options?: ScrollToOptions) => void;
 } = {}) {
   const promptMessages = makePromptExchangeMessages(5);
@@ -180,15 +154,6 @@ async function renderPromptRailViewport({
     ...(scrollTo ? { scrollTo: { configurable: true, value: scrollTo } } : {}),
   });
 
-  if (layout) {
-    stubElementRect(scroller, 0, layout.scrollerWidth);
-    stubElementRect(
-      screen.getByTestId("thread-message-column"),
-      layout.messageColumnLeft,
-      layout.messageColumnWidth,
-    );
-  }
-
   const promptEls = Array.from(
     container.querySelectorAll<HTMLElement>("[data-user-prompt-id]"),
   );
@@ -853,30 +818,6 @@ describe("ThreadViewport", () => {
     });
   });
 
-  it("positions the prompt rail in the gutter before the message column", async () => {
-    await renderPromptRailViewport({
-      layout: {
-        scrollerWidth: 1200,
-        messageColumnLeft: 180,
-        messageColumnWidth: 792,
-      },
-    });
-
-    expect(screen.getByLabelText("User prompt navigation")).toHaveStyle({ left: "124px" });
-  });
-
-  it("hides the prompt rail when the message column leaves no side gutter", async () => {
-    await renderPromptRailViewport({
-      layout: {
-        scrollerWidth: 560,
-        messageColumnLeft: 48,
-        messageColumnWidth: 480,
-      },
-    });
-
-    expect(screen.queryByLabelText("User prompt navigation")).not.toBeInTheDocument();
-  });
-
   it("opens a prompt navigator list and jumps to a selected prompt", async () => {
     const promptMessages = makeLongMessages(5);
     const { container } = render(<ViewportWithPromptNavigator messages={promptMessages} />);