diff --git a/src/components/CliOnlyScreen.test.tsx b/src/components/CliOnlyScreen.test.tsx
index 0812a4118..65cc00ea7 100644
--- a/src/components/CliOnlyScreen.test.tsx
+++ b/src/components/CliOnlyScreen.test.tsx
@@ -39,7 +39,7 @@ function cliOnlyCommands(
 
 const CLI_ONLY = cliOnlyCommands();
 
-describe("menus list command-line-only subcommands below a divider", () => {
+describe("menus separate mixed command groups with a divider", () => {
   test("the root menu", async () => {
     const r = renderScreen("/agentcore", { withContext: inProjectContext });
 
@@ -77,13 +77,14 @@ describe("menus list command-line-only subcommands below a divider", () => {
     r.unmount();
   });
 
-  test("a menu whose every subcommand is command line only", async () => {
+  test("a menu whose every subcommand is command line only has no redundant divider", async () => {
     const r = renderScreen("/agentcore/eval/ondemand");
 
-    await waitFor(() => hasCliDivider(r.lastFrame()!));
+    await waitForText(r.lastFrame, "❯ evaluate");
+    expect(hasCliDivider(r.lastFrame()!)).toBe(false);
     expect(menuEntries(r.lastFrame()!)).toEqual({
-      screens: [],
-      cliOnly: ["evaluate", "simulate"],
+      screens: ["evaluate", "simulate"],
+      cliOnly: [],
     });
     r.unmount();
   });
@@ -133,10 +134,12 @@ describe("every command-line-only command opens on screen", () => {
       const parent = command.parent!;
 
       if (command.commands.length > 0) {
-        // A group opens its own menu, with every child under the divider.
+        // A CLI-only group opens its own menu without a redundant separator.
         await waitForText(r.lastFrame, path.join(" → "));
-        await waitFor(() => hasCliDivider(r.lastFrame()!));
-        expect(menuEntries(r.lastFrame()!).screens).toEqual([]);
+        expect(hasCliDivider(r.lastFrame()!)).toBe(false);
+        expect(menuEntries(r.lastFrame()!).screens).toEqual(
+          command.commands.map((child) => child.name()),
+        );
       } else {
         await waitForText(r.lastFrame, "this command runs from the command line");
         const help = command.createHelp();
diff --git a/src/components/RouterScreen.test.tsx b/src/components/RouterScreen.test.tsx
index 7af18b3b4..f81a30231 100644
--- a/src/components/RouterScreen.test.tsx
+++ b/src/components/RouterScreen.test.tsx
@@ -64,6 +64,28 @@ function menuGroups(frame: string): { title: string | undefined; names: string[]
 // rendered frames — behavior a user would see, not internal state.
 
 describe("menu rendering", () => {
+  test.each([
+    "/agentcore/log",
+    "/agentcore/traces",
+    "/agentcore/harness/traces",
+    "/agentcore/runtime/traces",
+    "/agentcore/payment",
+    "/agentcore/payment/connector",
+    "/agentcore/payment/manager",
+    "/agentcore/payment/session",
+    "/agentcore/payment/instrument",
+  ])("%s has no extra divider above a CLI-only menu", async (path) => {
+    const r = renderScreen(path, { withContext: inProjectContext });
+    await waitForText(r.lastFrame, "type to choose a command");
+
+    const frame = r.lastFrame()!;
+    const lines = frame.split("\n");
+    const filterRow = lines.findIndex((line) => /^\s*\/ /.test(line));
+    expect(lines[filterRow + 2]).toMatch(/^\s*❯ /);
+    expect(hasCliDivider(frame)).toBe(false);
+    r.unmount();
+  });
+
   test("CLI-only command names use the same white and focused colors as other commands", () => {
     // A separate process keeps ANSI enabled without changing the plain-text screen tests.
     const result = spawnSync(
@@ -316,6 +338,21 @@ describe("narrow terminals", () => {
 });
 
 describe("filtering", () => {
+  test("removes the CLI-only divider when filtering leaves only that group and restores it", async () => {
+    const r = renderScreen("/agentcore");
+    await waitForText(r.lastFrame, "❯ create");
+    expect(hasCliDivider(r.lastFrame()!)).toBe(true);
+
+    await r.write("feedback");
+    await waitForText(r.lastFrame, "❯ feedback");
+    expect(hasCliDivider(r.lastFrame()!)).toBe(false);
+
+    for (const _ of "feedback") await r.press("backspace");
+    await waitForText(r.lastFrame, "❯ create");
+    expect(hasCliDivider(r.lastFrame()!)).toBe(true);
+    r.unmount();
+  });
+
   test("typing narrows the options to matches", async () => {
     const r = renderScreen("/agentcore/harness");
     await waitForText(r.lastFrame, "list");
@@ -433,6 +470,18 @@ describe("navigation", () => {
 describe("short terminals", () => {
   const ROWS = 15;
 
+  test("does not reserve a row for a redundant CLI-only divider", async () => {
+    const r = renderScreen("/agentcore/log", { withContext: inProjectContext });
+    await waitForText(r.lastFrame, "❯ runtime");
+    await r.resize(100, 8);
+
+    expect(r.lastFrame()).toContain("❯ runtime");
+    expect(r.lastFrame()).toContain("harness");
+    expect(r.lastFrame()).not.toContain("more");
+    expect(hasCliDivider(r.lastFrame()!)).toBe(false);
+    r.unmount();
+  });
+
   // fullMenu renders the root menu at the default height, where every option fits.
   async function fullMenu() {
     const r = renderScreen("/agentcore", { withContext: inProjectContext });
diff --git a/src/components/RouterScreen.tsx b/src/components/RouterScreen.tsx
index 47bea52c2..aab8c90fb 100644
--- a/src/components/RouterScreen.tsx
+++ b/src/components/RouterScreen.tsx
@@ -289,7 +289,10 @@ function CommandMenuBody({
   query,
   onQueryChange,
 }: CommandMenuBodyProps) {
-  const sections = useMemo(() => filtered.map((option) => option.section), [filtered]);
+  const sections = useMemo(() => {
+    const onlyCli = filtered.every((option) => option.section === CLI_ONLY_SECTION);
+    return filtered.map((option) => (onlyCli ? undefined : option.section));
+  }, [filtered]);
   const menuHeight = Math.max(0, contentRows - FILTER_ROWS - alertRows(alert, columns));
   const windowStart = Math.max(0, highlight - Math.floor(menuHeight / 2));
   const view = scrollWindow({