diff --git a/apps/web/src/components/ChatMarkdown.browser.test.tsx b/apps/web/src/components/ChatMarkdown.browser.test.tsx
index e30b81c5e5f93..c7a70bf51e317 100644
--- a/apps/web/src/components/ChatMarkdown.browser.test.tsx
+++ b/apps/web/src/components/ChatMarkdown.browser.test.tsx
@@ -91,6 +91,95 @@ function buttonsLabelled(container: HTMLElement, label: string) {
   );
 }
 
+describe("ChatMarkdown ordered list layout", () => {
+  it("preserves default-font indentation and wrapping when the markers already fit", async () => {
+    setup();
+    const container = document.createElement("div");
+    Object.assign(container.style, { font: "14px system-ui", width: "240px" });
+    await using screen = await render(
+      <ChatMarkdown
+        cwd={undefined}
+        text={
+          "1. A long list item whose text wraps over several lines at this width.\n2. Another item."
+        }
+      />,
+      { container },
+    );
+    const list = screen.container.querySelector("ol")!;
+    const item = list.querySelector("li")!;
+    const padding = getComputedStyle(list).paddingInlineStart;
+    const bounds = item.getBoundingClientRect();
+    list.style.setProperty("--list-gutter", "1.25rem");
+    expect(padding).toBe(getComputedStyle(list).paddingInlineStart);
+    expect(item.getBoundingClientRect().toJSON()).toEqual(bounds.toJSON());
+  });
+
+  it("keeps wide monospace markers inside the clipping edge, including nested lists", async () => {
+    setup();
+    const container = document.createElement("div");
+    Object.assign(container.style, { font: "22px monospace", width: "300px", overflow: "hidden" });
+    await using screen = await render(
+      <ChatMarkdown cwd={undefined} text={"1. First\n2. Second\n   1. Nested\n   2. Last"} />,
+      { container },
+    );
+    const probe = document.createElement("span");
+    const listStyle = getComputedStyle(screen.container.querySelector("ol")!);
+    probe.style.fontFamily = listStyle.fontFamily;
+    probe.style.fontSize = listStyle.fontSize;
+    probe.style.whiteSpace = "pre";
+    probe.textContent = "2. ";
+    container.append(probe);
+    const markerWidth = probe.getBoundingClientRect().width;
+    probe.remove();
+    expect(markerWidth).toBeGreaterThan(20);
+    for (const list of screen.container.querySelectorAll("ol")) {
+      const item = list.querySelector("li")!;
+      expect(item.getBoundingClientRect().left - markerWidth).toBeGreaterThanOrEqual(
+        list.getBoundingClientRect().left,
+      );
+    }
+  });
+
+  it("remeasures existing lists when the inherited interface font changes", async () => {
+    setup();
+    const container = document.createElement("div");
+    Object.assign(container.style, {
+      font: "22px var(--test-ordered-list-font, system-ui)",
+      width: "300px",
+    });
+    await using screen = await render(<ChatMarkdown cwd={undefined} text="1. First" />, {
+      container,
+    });
+    const list = screen.container.querySelector("ol")!;
+    const originalPadding = Number.parseFloat(getComputedStyle(list).paddingInlineStart);
+    try {
+      document.documentElement.style.setProperty("--test-ordered-list-font", "monospace");
+      await expect
+        .poll(() => Number.parseFloat(getComputedStyle(list).paddingInlineStart))
+        .toBeGreaterThan(originalPadding);
+      document.documentElement.style.removeProperty("--test-ordered-list-font");
+      await expect
+        .poll(() => Number.parseFloat(getComputedStyle(list).paddingInlineStart))
+        .toBe(originalPadding);
+    } finally {
+      document.documentElement.style.removeProperty("--test-ordered-list-font");
+    }
+  });
+
+  it("restores the single-digit gutter after reusing a list with wider numbers", async () => {
+    setup();
+    const markdown = (text: string) => <ChatMarkdown cwd={undefined} text={text} />;
+    await using screen = await render(markdown("1. First"));
+    const padding = () =>
+      Number.parseFloat(getComputedStyle(screen.container.querySelector("ol")!).paddingInlineStart);
+    const originalPadding = padding();
+    await screen.rerender(markdown("99. First\n100. Second"));
+    expect(padding()).toBeGreaterThan(originalPadding);
+    await screen.rerender(markdown("1. First"));
+    expect(padding()).toBe(originalPadding);
+  });
+});
+
 describe("ChatMarkdown favicon privacy", () => {
   it("suppresses private link images while preserving public links across updates", async () => {
     setup();
diff --git a/apps/web/src/components/ChatMarkdown.tsx b/apps/web/src/components/ChatMarkdown.tsx
index 91acb81d17304..fe2605315acf2 100644
--- a/apps/web/src/components/ChatMarkdown.tsx
+++ b/apps/web/src/components/ChatMarkdown.tsx
@@ -325,16 +325,87 @@ function findTaskListMarkerOffset(markdown: string, listItemStart: number): numb
   return listItemStart + firstLine.indexOf(match[1]);
 }
 
-function orderedListGutterStyle(
-  itemCount: number,
-  start: unknown,
-): { "--list-gutter": string } | undefined {
+function orderedListGutterStyle(itemCount: number, start: unknown) {
   const parsedStart = Number.parseInt(String(start ?? 1), 10);
   const firstNumber = Number.isNaN(parsedStart) ? 1 : parsedStart;
   const lastNumber = firstNumber + Math.max(itemCount - 1, 0);
   const markerWidth = Math.max(String(firstNumber).length, String(lastNumber).length);
-  if (markerWidth <= 1) return undefined;
-  return { "--list-gutter": `${markerWidth + 2}ch` };
+  return markerWidth > 1 ? { "--list-gutter": `${markerWidth + 2}ch` } : undefined;
+}
+
+function MarkdownOrderedList({
+  node,
+  start,
+  style,
+  ...props
+}: ComponentProps<"ol"> & ReactMarkdownExtraProps) {
+  const ref = useRef<HTMLOListElement>(null);
+  const itemCount =
+    node?.children?.filter((child) => child.type === "element" && child.tagName === "li").length ??
+    0;
+  const gutterStyle = orderedListGutterStyle(itemCount, start);
+  const hasWideMarker = gutterStyle !== undefined;
+
+  useLayoutEffect(() => {
+    const list = ref.current;
+    if (!list || hasWideMarker) return;
+    const measure = () => {
+      const marker = getComputedStyle(list.querySelector("li") ?? list, "::marker");
+      const probe = document.createElement("span");
+      Object.assign(probe.style, {
+        position: "fixed",
+        top: "0",
+        left: "0",
+        visibility: "hidden",
+        whiteSpace: "pre",
+        fontFamily: marker.fontFamily,
+        fontSize: marker.fontSize,
+        fontWeight: marker.fontWeight,
+        fontStyle: marker.fontStyle,
+        fontStretch: marker.fontStretch,
+        fontVariantNumeric: "tabular-nums",
+        fontFeatureSettings: marker.fontFeatureSettings,
+        fontVariationSettings: marker.fontVariationSettings,
+        letterSpacing: marker.letterSpacing,
+        wordSpacing: marker.wordSpacing,
+      });
+      // `ch` overestimates punctuation in proportional fonts. Measure the actual
+      // marker so fonts whose numbers already fit keep their indent and wrapping.
+      const markers = Array.from({ length: 10 }, (_, digit) => {
+        const span = document.createElement("span");
+        span.textContent = `${digit}. `;
+        probe.append(span);
+        return span;
+      });
+      document.body.append(probe);
+      const width = Math.ceil(
+        Math.max(...markers.map((span) => span.getBoundingClientRect().width)),
+      );
+      probe.remove();
+      list.style.setProperty("--list-gutter", `max(1.25rem, ${width}px)`);
+    };
+    measure();
+    // Appearance settings apply inherited fonts to the root after React commits.
+    const observer = new MutationObserver(measure);
+    observer.observe(document.documentElement, {
+      attributes: true,
+      attributeFilter: ["style", "class"],
+    });
+    document.fonts.addEventListener("loadingdone", measure);
+    return () => {
+      observer.disconnect();
+      document.fonts.removeEventListener("loadingdone", measure);
+    };
+  }, [hasWideMarker]);
+
+  return (
+    <ol
+      {...props}
+      ref={ref}
+      start={start}
+      style={gutterStyle ? { ...style, ...gutterStyle } : style}
+    />
+  );
 }
 
 const GITHUB_ALERT_PRESENTATIONS: Record<
@@ -994,15 +1065,7 @@ const CHAT_MARKDOWN_COMPONENTS = {
       </div>
     );
   },
-  ol: function MarkdownOrderedList({ node, start, style, ...props }) {
-    const itemCount =
-      node?.children?.filter((child) => child.type === "element" && child.tagName === "li")
-        .length ?? 0;
-    const gutterStyle = orderedListGutterStyle(itemCount, start);
-    return (
-      <ol {...props} start={start} style={gutterStyle ? { ...style, ...gutterStyle } : style} />
-    );
-  },
+  ol: MarkdownOrderedList,
   li: function MarkdownListItem({ node, children, ...props }) {
     const { skills } = use(ChatMarkdownRendererContext);
     // The checkbox finds its marker from this offset when toggled, so list items
diff --git a/apps/web/src/index.css b/apps/web/src/index.css
index 01fa601ab666e..be6d9fe61f8fe 100644
--- a/apps/web/src/index.css
+++ b/apps/web/src/index.css
@@ -1853,10 +1853,9 @@ code {
 }
 
 /* --list-gutter defaults to the same 1.25rem as .chat-markdown ul, but
-   ChatMarkdown's `ol` renderer widens it (via inline style) for lists whose
-   widest marker has multiple characters so it isn't clipped by list-style-position:
-   outside painting the marker past the padding box. Reset it here too so a
-   nested ol without its own widened marker doesn't inherit the outer one. */
+   ChatMarkdown's `ol` renderer measures single-digit markers and widens it only
+   when needed. Multi-digit lists use a digit-count-based `ch` gutter. Reset it
+   here too so nested lists don't inherit their parent's widened gutter. */
 :is(.chat-markdown, .composer-tiptap) ol {
   --list-gutter: 1.25rem;
   padding-inline-start: var(--list-gutter, 1.25rem);