diff --git a/webui/src/components/thread/PromptRail.tsx b/webui/src/components/thread/PromptRail.tsx
index b7278f3f..6714ed2c 100644
--- a/webui/src/components/thread/PromptRail.tsx
+++ b/webui/src/components/thread/PromptRail.tsx
@@ -1,11 +1,4 @@
-import {
-  type RefObject,
-  useCallback,
-  useEffect,
-  useMemo,
-  useRef,
-  useState,
-} from "react";
+import { type RefObject, useCallback, useEffect, useMemo, useRef, useState } from "react";
 
 import { cn } from "@/lib/utils";
 import type { UIMessage } from "@/lib/types";
@@ -29,6 +22,7 @@ interface MeasuredPrompt extends PromptAnchor {
 }
 
 interface PromptMarker {
+  answerPreview: string;
   count: number;
   ids: string[];
   label: string;
@@ -43,10 +37,11 @@ const DENSE_BUCKET_HEIGHT_PX = 12;
 const DENSE_BUCKET_FALLBACK_COUNT = 32;
 const DENSE_BUCKET_MAX_COUNT = 42;
 const MARKER_MIN_GAP_PX = 9;
-const MARKER_BASE_WIDTH_PX = 16;
-const MARKER_MAX_WIDTH_PX = 28;
+const MARKER_BASE_WIDTH_PX = 9;
+const MARKER_STACK_GAP_PX = 16;
+const RAIL_FALLBACK_HEIGHT_PX = 300;
 const MEASURE_RETRY_FRAMES = 4;
-const RAIL_REVEAL_MS = 1400;
+const HOVER_MARKER_WIDTHS_PX = [28, 22, 16, 11];
 
 export function PromptRail({
   bottomOffset,
@@ -57,22 +52,12 @@ export function PromptRail({
   const promptAnchors = useMemo(() => userPromptAnchors(messages), [messages]);
   const [markers, setMarkers] = useState<PromptMarker[]>([]);
   const [activePromptId, setActivePromptId] = useState<string | null>(null);
-  const [revealed, setRevealed] = useState(false);
-  const revealTimeoutRef = useRef<number | null>(null);
-
-  const revealTemporarily = useCallback(() => {
-    setRevealed(true);
-    if (revealTimeoutRef.current !== null) {
-      window.clearTimeout(revealTimeoutRef.current);
-    }
-    revealTimeoutRef.current = window.setTimeout(() => {
-      setRevealed(false);
-      revealTimeoutRef.current = null;
-    }, RAIL_REVEAL_MS);
-  }, []);
+  const [focusedMarkerIndex, setFocusedMarkerIndex] = useState<number | null>(null);
 
   const updateMarkers = useCallback(() => {
     const scrollEl = scrollRef.current;
+    const nextRailHeight = railRef.current?.clientHeight ?? 0;
+
     if (!scrollEl || promptAnchors.length < MIN_PROMPTS_FOR_RAIL) {
       setMarkers([]);
       setActivePromptId(null);
@@ -87,7 +72,8 @@ export function PromptRail({
     }
 
     const measured = measurePrompts(scrollEl, promptAnchors, scrollRange);
-    setMarkers(groupPromptMarkers(measured, railRef.current?.clientHeight ?? 0));
+    const grouped = groupPromptMarkers(measured, nextRailHeight);
+    setMarkers(distributeMarkerPositions(grouped, nextRailHeight));
     setActivePromptId(activePromptForScroll(measured, scrollEl.scrollTop));
   }, [promptAnchors, scrollRef]);
 
@@ -112,7 +98,6 @@ export function PromptRail({
     let frame = 0;
     const schedule = () => {
       window.cancelAnimationFrame(frame);
-      revealTemporarily();
       frame = window.requestAnimationFrame(updateMarkers);
     };
 
@@ -123,7 +108,7 @@ export function PromptRail({
       scrollEl.removeEventListener("scroll", schedule);
       window.removeEventListener("resize", schedule);
     };
-  }, [revealTemporarily, scrollRef, updateMarkers]);
+  }, [scrollRef, updateMarkers]);
 
   useEffect(() => {
     const scrollEl = scrollRef.current;
@@ -134,77 +119,72 @@ export function PromptRail({
     return () => observer.disconnect();
   }, [scrollRef, updateMarkers]);
 
-  useEffect(() => {
-    return () => {
-      if (revealTimeoutRef.current !== null) {
-        window.clearTimeout(revealTimeoutRef.current);
-      }
-    };
-  }, []);
-
   if (markers.length === 0) return null;
 
-  const maxMarkerCount = Math.max(...markers.map((marker) => marker.count));
-  const activeMarkerIndex = markers.findIndex((marker) =>
-    marker.ids.includes(activePromptId ?? ""),
-  );
-
   return (
     <div
       ref={railRef}
       aria-label="User prompt navigation"
       className={cn(
-        "group pointer-events-auto absolute right-4 top-14 z-20 hidden w-8 opacity-70 md:block",
-        "transition-opacity duration-200 hover:opacity-100",
+        "group pointer-events-auto absolute left-7 top-3 z-20 hidden w-9 opacity-100 md:block",
+        "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) }}
     >
       {markers.map((marker, index) => {
         const active = marker.ids.includes(activePromptId ?? "");
-        const nearActive = activeMarkerIndex < 0 || Math.abs(index - activeMarkerIndex) <= 1;
+        const hoverDistance =
+          focusedMarkerIndex === null ? null : Math.abs(index - focusedMarkerIndex);
         return (
           <button
             key={marker.ids.join("|")}
             type="button"
             aria-label={`Jump to prompt: ${marker.label}`}
             onClick={() => jumpToPrompt(scrollRef.current, marker.ids[marker.ids.length - 1])}
+            onBlur={() => setFocusedMarkerIndex(null)}
+            onFocus={() => setFocusedMarkerIndex(index)}
+            onPointerEnter={() => setFocusedMarkerIndex(index)}
+            onPointerLeave={() => setFocusedMarkerIndex(null)}
             className={cn(
-              "group/marker absolute right-0 h-5 -translate-y-1/2 overflow-visible rounded-full",
+              "group/marker absolute left-0 h-4 w-9 -translate-y-1/2 overflow-visible rounded-sm",
               "focus-visible:outline-none focus-visible:ring-2 focus-visible:ring-blue-400/60",
             )}
-            style={{
-              top: `${marker.topPercent}%`,
-              width: markerWidth(marker.count, maxMarkerCount, active),
-            }}
+            style={{ top: `${marker.topPercent}%` }}
           >
             <span
               aria-hidden
+              data-testid="prompt-rail-marker"
               className={cn(
-                "absolute right-0 top-1/2 h-[3px] w-full -translate-y-1/2 rounded-full",
-                "bg-foreground/20 transition-[background-color,opacity,transform,height] duration-200",
-                "group-hover/marker:bg-blue-500/70 group-hover/marker:opacity-100 group-hover/marker:scale-x-110",
-                "group-focus-visible/marker:bg-blue-500 group-focus-visible/marker:opacity-100 group-focus-visible/marker:scale-x-110",
-                marker.count > 1 && "bg-foreground/30",
-                active && "h-1 bg-foreground/65 opacity-80 shadow-sm",
-                !active && nearActive && "opacity-25 group-hover:opacity-55",
-                !active && !nearActive && !revealed && "opacity-0 group-hover:opacity-40",
-                !active && !nearActive && revealed && "opacity-35",
+                "absolute left-0 top-1/2 h-0.5 -translate-y-1/2 rounded-full",
+                "transition-[width,background-color,opacity,height] duration-150",
+                railMarkerTone(hoverDistance, active),
               )}
+              style={{
+                height: markerHeight(hoverDistance),
+                width: markerWidth(hoverDistance),
+              }}
             />
             <span
               aria-hidden
               className={cn(
-                "pointer-events-none absolute right-9 top-1/2 z-30 w-64 -translate-y-1/2 rounded-lg px-3 py-2 text-left",
-                "bg-background/95 text-xs leading-5 text-foreground shadow-lg ring-1 ring-border/80 backdrop-blur",
-                "opacity-0 translate-x-1 transition-[opacity,transform] duration-150",
-                "group-hover/marker:opacity-100 group-hover/marker:translate-x-0",
-                "group-focus-visible/marker:opacity-100 group-focus-visible/marker:translate-x-0",
+                "pointer-events-none absolute left-10 top-1/2 z-30 w-[34rem] max-w-[calc(100vw-4rem)] -translate-y-1/2 rounded-[20px] px-4 py-3 text-left",
+                "border border-border/70 bg-popover/95 text-popover-foreground shadow-[0_18px_45px_rgba(0,0,0,0.12)] backdrop-blur-xl",
+                "dark:border-white/10 dark:bg-[#2f2f2f]/95 dark:text-white dark:shadow-[0_18px_45px_rgba(0,0,0,0.45)]",
+                "-translate-x-2 scale-[0.98] opacity-0 transition-[opacity,transform] duration-150",
+                "group-hover/marker:translate-x-0 group-hover/marker:scale-100 group-hover/marker:opacity-100",
+                "group-focus-visible/marker:translate-x-0 group-focus-visible/marker:scale-100 group-focus-visible/marker:opacity-100",
               )}
             >
-              <span className="block max-h-24 overflow-hidden whitespace-pre-wrap break-words">
+              <span className="line-clamp-2 whitespace-pre-wrap break-words text-[15px] font-semibold leading-6">
                 {marker.preview}
               </span>
+              {marker.answerPreview ? (
+                <span className="mt-1.5 line-clamp-3 whitespace-pre-wrap break-words text-[14px] leading-6 text-muted-foreground dark:text-white/55">
+                  {marker.answerPreview}
+                </span>
+              ) : null}
             </span>
           </button>
         );
@@ -250,10 +230,12 @@ function groupPromptMarkers(
       last.count += 1;
       last.ids.push(prompt.id);
       last.label = groupedPromptLabel(last.count, prompt.label);
-      last.preview = groupedPromptPreview(last.count, prompt.preview);
+      last.answerPreview = prompt.answerPreview;
+      last.preview = prompt.preview;
       continue;
     }
     groups.push({
+      answerPreview: prompt.answerPreview,
       count: 1,
       ids: [prompt.id],
       label: prompt.label,
@@ -298,14 +280,30 @@ function bucketPromptMarkers(
       label: bucket.length === 1
         ? latest.label
         : groupedPromptLabel(bucket.length, latest.label),
-      preview: bucket.length === 1
-        ? latest.preview
-        : groupedPromptPreview(bucket.length, latest.preview),
+      answerPreview: latest.answerPreview,
+      preview: latest.preview,
       topPercent,
     }];
   });
 }
 
+function distributeMarkerPositions(markers: PromptMarker[], railHeight: number): PromptMarker[] {
+  const height = railHeight > 0 ? railHeight : RAIL_FALLBACK_HEIGHT_PX;
+  if (markers.length <= 1) {
+    return markers.map((marker) => ({ ...marker, topPercent: 50 }));
+  }
+
+  const availableHeight = Math.max(0, height - MARKER_STACK_GAP_PX);
+  const stepPx = Math.min(MARKER_STACK_GAP_PX, availableHeight / (markers.length - 1));
+  const stackHeight = stepPx * (markers.length - 1);
+  const firstMarkerPx = (height - stackHeight) / 2;
+
+  return markers.map((marker, index) => ({
+    ...marker,
+    topPercent: ((firstMarkerPx + stepPx * index) / height) * 100,
+  }));
+}
+
 function activePromptForScroll(
   measured: MeasuredPrompt[],
   scrollTop: number,
@@ -327,16 +325,26 @@ function groupedPromptLabel(count: number, latestLabel: string): string {
   return `${count} prompts, latest: ${latestLabel}`;
 }
 
-function groupedPromptPreview(count: number, latestPreview: string): string {
-  return `${count} prompts\n\n${latestPreview}`;
+function markerWidth(hoverDistance: number | null): number {
+  if (hoverDistance === null) return MARKER_BASE_WIDTH_PX;
+  return HOVER_MARKER_WIDTHS_PX[hoverDistance] ?? MARKER_BASE_WIDTH_PX;
 }
 
-function markerWidth(count: number, maxCount: number, active: boolean): number {
-  if (maxCount <= 1) return active ? 34 : MARKER_BASE_WIDTH_PX;
-  const density = Math.log2(count + 1) / Math.log2(maxCount + 1);
-  const width = MARKER_BASE_WIDTH_PX
-    + (MARKER_MAX_WIDTH_PX - MARKER_BASE_WIDTH_PX) * density;
-  return Math.round(active ? width + 4 : width);
+function markerHeight(hoverDistance: number | null): number {
+  return hoverDistance === 0 ? 3 : 2;
+}
+
+function railMarkerTone(hoverDistance: number | null, active: boolean): string {
+  if (hoverDistance === 0) {
+    return "bg-[#222222] opacity-100 dark:bg-white";
+  }
+  if (hoverDistance !== null && hoverDistance < HOVER_MARKER_WIDTHS_PX.length) {
+    return "bg-[#d0d0d0] opacity-100 dark:bg-white/35";
+  }
+  if (active) {
+    return "bg-[#6f6f6f] opacity-100 dark:bg-white/55";
+  }
+  return "bg-[#d8d8d8] opacity-100 dark:bg-white/25";
 }
 
 function clamp(value: number, min: number, max: number): number {
diff --git a/webui/src/components/thread/promptNavigation.ts b/webui/src/components/thread/promptNavigation.ts
index 17b1b762..7aeca8ac 100644
--- a/webui/src/components/thread/promptNavigation.ts
+++ b/webui/src/components/thread/promptNavigation.ts
@@ -1,6 +1,7 @@
 import type { UIMessage } from "@/lib/types";
 
 export interface PromptAnchor {
+  answerPreview: string;
   id: string;
   label: string;
   preview: string;
@@ -10,9 +11,10 @@ export interface PromptAnchor {
 
 export function userPromptAnchors(messages: UIMessage[]): PromptAnchor[] {
   let index = 0;
-  return messages.flatMap((message) => {
+  return messages.flatMap((message, messageIndex) => {
     if (message.role !== "user") return [];
     const anchor: PromptAnchor = {
+      answerPreview: nextAssistantPreview(messages, messageIndex),
       id: message.id,
       label: promptLabel(message.content, index),
       preview: promptPreview(message.content, index),
@@ -27,13 +29,34 @@ export function userPromptAnchors(messages: UIMessage[]): PromptAnchor[] {
 export function promptLabel(content: string, index: number): string {
   const text = content.replace(/\s+/g, " ").trim();
   if (!text) return `Prompt ${index + 1}`;
-  return text.length > 80 ? `${text.slice(0, 77)}...` : text;
+  return truncatePreview(text, 80);
 }
 
 export function promptPreview(content: string, index: number): string {
-  const text = content.replace(/\n{3,}/g, "\n\n").trim();
+  const text = compactPreview(content);
   if (!text) return `Prompt ${index + 1}`;
-  return text.length > 320 ? `${text.slice(0, 317)}...` : text;
+  return truncatePreview(text, 320);
+}
+
+function nextAssistantPreview(messages: UIMessage[], promptIndex: number): string {
+  for (let index = promptIndex + 1; index < messages.length; index += 1) {
+    const message = messages[index];
+    if (message.role === "user") return "";
+    if (message.role !== "assistant") continue;
+
+    const preview = truncatePreview(compactPreview(message.content), 240);
+    if (preview) return preview;
+  }
+
+  return "";
+}
+
+function compactPreview(content: string): string {
+  return content.replace(/\n{3,}/g, "\n\n").trim();
+}
+
+function truncatePreview(text: string, maxLength: number): string {
+  return text.length > maxLength ? `${text.slice(0, maxLength - 3)}...` : text;
 }
 
 export function jumpToPrompt(scrollEl: HTMLElement | null, promptId: string | undefined): void {
diff --git a/webui/src/tests/thread-viewport.test.tsx b/webui/src/tests/thread-viewport.test.tsx
index 301dea8c..7450a5fd 100644
--- a/webui/src/tests/thread-viewport.test.tsx
+++ b/webui/src/tests/thread-viewport.test.tsx
@@ -91,6 +91,23 @@ function makeLongMessages(count: number): UIMessage[] {
   }));
 }
 
+function makePromptExchangeMessages(count: number): UIMessage[] {
+  return Array.from({ length: count }, (_, index) => ([
+    {
+      id: `m${index}`,
+      role: "user" as const,
+      content: `message ${index}`,
+      createdAt: index * 2,
+    },
+    {
+      id: `a${index}`,
+      role: "assistant" as const,
+      content: `answer ${index}`,
+      createdAt: index * 2 + 1,
+    },
+  ])).flat();
+}
+
 function ViewportWithPromptNavigator({ messages }: { messages: UIMessage[] }) {
   const viewportRef = useRef<ThreadViewportHandle | null>(null);
   return (
@@ -604,7 +621,7 @@ describe("ThreadViewport", () => {
       screen.queryByText(`message ${firstVisible - 1}`),
     ).not.toBeInTheDocument();
     expect(screen.getByText(`message ${firstVisible}`)).toBeInTheDocument();
-    expect(screen.getByText("message 299")).toBeInTheDocument();
+    expect(screen.getAllByText("message 299").length).toBeGreaterThan(0);
   });
 
   it("automatically requests older transcript pages near the top", () => {
@@ -635,7 +652,7 @@ describe("ThreadViewport", () => {
   });
 
   it("renders a prompt rail that jumps to user messages", async () => {
-    const promptMessages = makeLongMessages(5);
+    const promptMessages = makePromptExchangeMessages(5);
     const { container } = render(
       <ThreadViewport
         messages={promptMessages}
@@ -670,9 +687,31 @@ describe("ThreadViewport", () => {
     });
 
     expect(screen.getByLabelText("User prompt navigation")).toBeInTheDocument();
+    const promptMarkers = screen.getAllByRole("button", { name: /Jump to prompt:/ });
+    const markerTops = promptMarkers.map((marker) => Number.parseFloat(marker.style.top));
+    expect(markerTops[2]).toBeCloseTo(50);
+    expect(markerTops[1] - markerTops[0]).toBeCloseTo(16 / 3);
+    expect(markerTops[4] - markerTops[0]).toBeCloseTo(64 / 3);
+
+    const railMarkers = screen.getAllByTestId("prompt-rail-marker");
+    expect(railMarkers).toHaveLength(promptMarkers.length);
+    expect(railMarkers.every((marker) => marker.style.width === "9px")).toBe(true);
+
+    fireEvent.pointerEnter(promptMarkers[2]);
+    expect(railMarkers.map((marker) => marker.style.width)).toEqual([
+      "16px",
+      "22px",
+      "28px",
+      "22px",
+      "16px",
+    ]);
+
+    fireEvent.pointerLeave(promptMarkers[2]);
+    expect(railMarkers.every((marker) => marker.style.width === "9px")).toBe(true);
 
     const targetPrompt = screen.getByRole("button", { name: "Jump to prompt: message 3" });
     expect(within(targetPrompt).getByText("message 3")).toBeInTheDocument();
+    expect(within(targetPrompt).getByText("answer 3")).toBeInTheDocument();
 
     fireEvent.click(targetPrompt);