diff --git a/apps/native/src/components/widget/promptinput/mac-recommendation-chip.tsx b/apps/native/src/components/widget/promptinput/mac-recommendation-chip.tsx
index ce6bd8bda..f99d47d76 100644
--- a/apps/native/src/components/widget/promptinput/mac-recommendation-chip.tsx
+++ b/apps/native/src/components/widget/promptinput/mac-recommendation-chip.tsx
@@ -3,9 +3,8 @@
 import { BadgeButton } from "@/components/ui/badge-button";
 import { useRecommendedPrompt } from "@/hooks/use-recommended-prompt";
 import { getTelemetry } from "@/lib/telemetry/instance";
-import { uiActions } from "@nixmac/state";
 
-export function MacRecommendationChip() {
+export function MacRecommendationChip({ onSelect }: { onSelect: (prompt: string) => void }) {
   const { recommendation } = useRecommendedPrompt();
 
   if (!recommendation) return null;
@@ -18,7 +17,7 @@ export function MacRecommendationChip() {
           name: "prompt_suggestion_used",
           props: { surface: "mac_recommendation" },
         });
-        uiActions.setEvolvePrompt(recommendation.promptText);
+        onSelect(recommendation.promptText);
       }}
     >
       {recommendation.promptText}
diff --git a/apps/native/src/components/widget/promptinput/prompt-history-badge.tsx b/apps/native/src/components/widget/promptinput/prompt-history-badge.tsx
index 0a43f65ae..85c8a97ff 100644
--- a/apps/native/src/components/widget/promptinput/prompt-history-badge.tsx
+++ b/apps/native/src/components/widget/promptinput/prompt-history-badge.tsx
@@ -12,14 +12,15 @@ import {
 import { Popover, PopoverContent, PopoverTrigger } from "@/components/ui/popover";
 import { getTelemetry } from "@/lib/telemetry/instance";
 import { cn } from "@/lib/utils";
-import { uiActions, useUiState, useViewModel } from "@nixmac/state";
+import { useUiState, useViewModel } from "@nixmac/state";
 import { ClockIcon } from "lucide-react";
-import { useState } from "react";
+import { useRef, useState } from "react";
 
-export function PromptHistoryBadge() {
+export function PromptHistoryBadge({ onSelect }: { onSelect: (prompt: string) => void }) {
+  const focusPromptAfterCloseRef = useRef(false);
   const history = useViewModel((s) => s.promptHistory);
   const evolvePrompt = useUiState((s) => s.evolvePrompt);
-    const isProcessing = useUiState((s) => s.isProcessing);
+  const isProcessing = useUiState((s) => s.isProcessing);
   const processingAction = useUiState((s) => s.processingAction);
 
   const disabled = isProcessing && processingAction === "evolve";
@@ -36,7 +37,8 @@ export function PromptHistoryBadge() {
       name: "prompt_suggestion_used",
       props: { surface: "history" },
     });
-    uiActions.setEvolvePrompt(prompt);
+    focusPromptAfterCloseRef.current = true;
+    onSelect(prompt);
     setOpen(false);
     setSearchValue("");
   };
@@ -60,7 +62,16 @@ export function PromptHistoryBadge() {
           My History
         </BadgeButton>
       </PopoverTrigger>
-      <PopoverContent className="w-[400px] p-0" align="start">
+      <PopoverContent
+        className="w-[400px] p-0"
+        align="start"
+        onCloseAutoFocus={(event) => {
+          if (!focusPromptAfterCloseRef.current) return;
+
+          focusPromptAfterCloseRef.current = false;
+          event.preventDefault();
+        }}
+      >
         <Command shouldFilter={false}>
           <CommandInput
             placeholder="Search history..."
diff --git a/apps/native/src/components/widget/promptinput/prompt-input.test.tsx b/apps/native/src/components/widget/promptinput/prompt-input.test.tsx
index 9552964fd..f3cd73532 100644
--- a/apps/native/src/components/widget/promptinput/prompt-input.test.tsx
+++ b/apps/native/src/components/widget/promptinput/prompt-input.test.tsx
@@ -1,5 +1,5 @@
 import "@testing-library/jest-dom";
-import { fireEvent, render, screen, waitFor } from "@testing-library/react";
+import { act, fireEvent, render, screen, waitFor } from "@testing-library/react";
 import { afterEach, beforeEach, describe, expect, it, vi } from "vitest";
 
 import { PromptInput } from "@/components/widget/promptinput/prompt-input";
@@ -15,6 +15,7 @@ const mocks = vi.hoisted(() => ({
   buildCheck: vi.fn<() => Promise<{ passed: boolean }>>(),
   getPrefs: vi.fn<() => Promise<Record<string, never>>>(),
   checkTools: vi.fn<() => Promise<{ claude: boolean; codex: boolean; opencode: boolean }>>(),
+  getRecommendedPrompt: vi.fn<() => Promise<null>>(),
 }));
 
 vi.mock("@/hooks/use-evolve", () => ({
@@ -25,18 +26,10 @@ vi.mock("@/hooks/use-evolve", () => ({
   }),
 }));
 
-vi.mock("@/components/widget/promptinput/mac-recommendation-chip", () => ({
-  MacRecommendationChip: () => null,
-}));
-
 vi.mock("@/components/widget/promptinput/homebrew-badge", () => ({
   HomebrewBadge: () => null,
 }));
 
-vi.mock("@/components/widget/promptinput/prompt-history-badge", () => ({
-  PromptHistoryBadge: () => null,
-}));
-
 vi.mock("@/components/widget/promptinput/system-defaults-cta", () => ({
   SystemDefaultsCTA: () => null,
 }));
@@ -45,9 +38,9 @@ vi.mock("@/components/widget/promptinput/system-defaults-cta", () => ({
 // (router.tsx → DarwinWidget → EditorPanel → monaco, which needs matchMedia).
 vi.mock("@/router", () => ({
   nav: {
-    openSettings: vi.fn(),
-    goHome: vi.fn(),
-    closeSettings: vi.fn(),
+    openSettings: vi.fn<() => void>(),
+    goHome: vi.fn<() => void>(),
+    closeSettings: vi.fn<() => void>(),
   },
 }));
 
@@ -69,6 +62,9 @@ vi.mock("@/ipc/api", () => ({
     cli: {
       checkTools: mocks.checkTools,
     },
+    scanner: {
+      getRecommendedPrompt: mocks.getRecommendedPrompt,
+    },
   },
 }));
 
@@ -83,19 +79,32 @@ const dirtyGitStatus: GitStatus = {
   changes: [],
 };
 
+const scrollIntoView = vi.fn<(options?: ScrollIntoViewOptions | boolean) => void>();
+const originalScrollIntoView = Element.prototype.scrollIntoView;
+
+class ResizeObserverStub {
+  observe() {}
+  unobserve() {}
+  disconnect() {}
+}
+
 function resetStore() {
-  uiActions.setEvolvePrompt("");
-  viewModelActions.setState({
-    git: null,
-    evolve: null,
-    build: {
-      externalBuildDetected: false,
-      upstreamUpdateAvailable: false,
-      rebuildNeeded: false,
-    },
-    preferences: makeGlobalPreferences(),
+  act(() => {
+    uiActions.setEvolvePrompt("");
+    uiActions.setRecommendedPrompt(null);
+    viewModelActions.setState({
+      git: null,
+      evolve: null,
+      build: {
+        externalBuildDetected: false,
+        upstreamUpdateAvailable: false,
+        rebuildNeeded: false,
+      },
+      preferences: makeGlobalPreferences(),
+      promptHistory: [],
+    });
+    uiActions.setProcessing(false);
   });
-  uiActions.setProcessing(false);
 }
 
 async function settleProviderValidation() {
@@ -107,16 +116,26 @@ async function settleProviderValidation() {
 
 describe("<PromptInput>", () => {
   beforeEach(() => {
+    Element.prototype.scrollIntoView = scrollIntoView;
+    vi.stubGlobal("ResizeObserver", ResizeObserverStub);
     resetStore();
     mocks.handleEvolve.mockResolvedValue();
     mocks.evolveFromManual.mockResolvedValue();
     mocks.buildCheck.mockResolvedValue({ passed: true });
     mocks.getPrefs.mockResolvedValue({});
     mocks.checkTools.mockResolvedValue({ claude: false, codex: false, opencode: false });
+    mocks.getRecommendedPrompt.mockResolvedValue(null);
   });
 
   afterEach(() => {
     resetStore();
+    scrollIntoView.mockReset();
+    if (originalScrollIntoView) {
+      Element.prototype.scrollIntoView = originalScrollIntoView;
+    } else {
+      Reflect.deleteProperty(Element.prototype, "scrollIntoView");
+    }
+    vi.unstubAllGlobals();
     vi.clearAllMocks();
   });
 
@@ -135,7 +154,7 @@ describe("<PromptInput>", () => {
     expect(screen.queryByRole("dialog")).not.toBeInTheDocument();
   });
 
-  it("seeds a full starter prompt from the curated chips", async () => {
+  it("reveals and focuses a seeded starter prompt without submitting it", async () => {
     // The default suggestion variant is `spotlight`; force `chips` via the
     // developer override so the curated chips render for this scenario.
     viewModelActions.patch({
@@ -155,6 +174,100 @@ describe("<PromptInput>", () => {
 
     fireEvent.click(chip);
 
-    expect(screen.getByTestId("evolve-prompt-input")).toHaveValue(suggestion.prompt);
+    const input = screen.getByTestId("evolve-prompt-input") as HTMLTextAreaElement;
+
+    await waitFor(() => {
+      expect(input).toHaveValue(suggestion.prompt);
+      expect(scrollIntoView).toHaveBeenCalledWith({ behavior: "smooth", block: "nearest" });
+      expect(input).toHaveFocus();
+    });
+    expect(input.selectionStart).toBe(suggestion.prompt.length);
+    expect(input.selectionEnd).toBe(suggestion.prompt.length);
+    expect(mocks.handleEvolve).not.toHaveBeenCalled();
+  });
+
+  it("keeps focus on a prompt selected from history after the popover closes", async () => {
+    const historyPrompt = "Show all file extensions in Finder";
+    viewModelActions.setState({ promptHistory: [historyPrompt] });
+
+    render(<PromptInput />);
+    await settleProviderValidation();
+
+    fireEvent.click(screen.getByRole("button", { name: "My History" }));
+    fireEvent.click(await screen.findByText(historyPrompt));
+
+    const input = screen.getByTestId("evolve-prompt-input") as HTMLTextAreaElement;
+    await waitFor(() => {
+      expect(screen.queryByPlaceholderText("Search history...")).not.toBeInTheDocument();
+      expect(input).toHaveValue(historyPrompt);
+      expect(scrollIntoView).toHaveBeenCalledWith({ behavior: "smooth", block: "nearest" });
+      expect(input).toHaveFocus();
+    });
+    expect(input.selectionStart).toBe(historyPrompt.length);
+    expect(input.selectionEnd).toBe(historyPrompt.length);
+    expect(mocks.handleEvolve).not.toHaveBeenCalled();
+  });
+
+  it("restores focus to the history trigger when the popover closes without a selection", async () => {
+    viewModelActions.setState({ promptHistory: ["Show all file extensions in Finder"] });
+
+    render(<PromptInput />);
+    await settleProviderValidation();
+
+    const trigger = screen.getByRole("button", { name: "My History" });
+    fireEvent.click(trigger);
+
+    const search = await screen.findByPlaceholderText("Search history...");
+    await waitFor(() => expect(search).toHaveFocus());
+    fireEvent.keyDown(search, { key: "Escape" });
+
+    await waitFor(() => {
+      expect(screen.queryByPlaceholderText("Search history...")).not.toBeInTheDocument();
+      expect(trigger).toHaveFocus();
+    });
+  });
+
+  it("routes the Mac recommendation through the same seed behavior", async () => {
+    const recommendation = {
+      id: "finder-extensions",
+      promptText: "Show all file extensions in Finder",
+    };
+    uiActions.setRecommendedPrompt(recommendation);
+
+    render(<PromptInput />);
+    await settleProviderValidation();
+
+    fireEvent.click(screen.getByRole("button", { name: recommendation.promptText }));
+
+    const input = screen.getByTestId("evolve-prompt-input") as HTMLTextAreaElement;
+    await waitFor(() => {
+      expect(input).toHaveValue(recommendation.promptText);
+      expect(scrollIntoView).toHaveBeenCalled();
+      expect(input).toHaveFocus();
+    });
+    expect(input.selectionStart).toBe(recommendation.promptText.length);
+    expect(input.selectionEnd).toBe(recommendation.promptText.length);
+    expect(mocks.handleEvolve).not.toHaveBeenCalled();
+  });
+
+  it("avoids smooth scrolling when reduced motion is preferred", async () => {
+    vi.stubGlobal("matchMedia", vi.fn().mockReturnValue({ matches: true }));
+    viewModelActions.patch({
+      preferences: makeGlobalPreferences({
+        featureFlagOverrides: { [EVOLVE_PROMPT_SUGGESTIONS_FLAG]: "chips" },
+      }),
+    });
+
+    const suggestion = STARTER_PROMPT_CHIPS.find(({ id }) => id === "dev-terminal");
+    if (!suggestion) throw new Error("Expected dev-terminal starter prompt");
+
+    render(<PromptInput />);
+    await settleProviderValidation();
+
+    fireEvent.click(screen.getByRole("button", { name: suggestion.label }));
+
+    await waitFor(() => {
+      expect(scrollIntoView).toHaveBeenCalledWith({ behavior: "auto", block: "nearest" });
+    });
   });
 });
diff --git a/apps/native/src/components/widget/promptinput/prompt-input.tsx b/apps/native/src/components/widget/promptinput/prompt-input.tsx
index 7dd58f212..4231495a1 100644
--- a/apps/native/src/components/widget/promptinput/prompt-input.tsx
+++ b/apps/native/src/components/widget/promptinput/prompt-input.tsx
@@ -30,11 +30,12 @@ import { getTelemetry } from "@/lib/telemetry/instance";
 import { nav } from "@/router";
 import { uiActions, useUiState, useViewModel } from "@nixmac/state";
 import { ArrowUpIcon } from "lucide-react";
-import { useEffect, useState } from "react";
+import { useEffect, useRef, useState } from "react";
 
 const MAX_CONTEXT_LENGTH = 1000;
 
 export function PromptInput() {
+  const promptInputRef = useRef<HTMLTextAreaElement>(null);
   const evolvePrompt = useUiState((s) => s.evolvePrompt);
   const isProcessing = useUiState((s) => s.isProcessing);
   const processingAction = useUiState((s) => s.processingAction);
@@ -141,7 +142,23 @@ export function PromptInput() {
 
   // PostHog-flag-driven suggestion surface under the input.
   const suggestionsVariant = usePromptSuggestionsVariant();
-  const seedPrompt = (prompt: string) => uiActions.setEvolvePrompt(prompt);
+  const seedPrompt = (prompt: string) => {
+    uiActions.setEvolvePrompt(prompt);
+
+    requestAnimationFrame(() => {
+      const input = promptInputRef.current;
+      if (!input || input.disabled) return;
+
+      const prefersReducedMotion =
+        window.matchMedia?.("(prefers-reduced-motion: reduce)").matches ?? false;
+      input.scrollIntoView({
+        behavior: prefersReducedMotion ? "auto" : "smooth",
+        block: "nearest",
+      });
+      input.focus({ preventScroll: true });
+      input.setSelectionRange(input.value.length, input.value.length);
+    });
+  };
 
   const words = evolvePrompt.split(" ").length;
   const percentage = words / MAX_CONTEXT_LENGTH;
@@ -152,6 +169,7 @@ export function PromptInput() {
     <div className="space-y-3 flex-col min-h-24">
       <InputGroup className="bg-background flex-col min-h-24">
         <InputGroupTextarea
+          ref={promptInputRef}
           id="evolve-prompt-input"
           data-testid="evolve-prompt-input"
           disabled={isLoading}
@@ -240,12 +258,12 @@ export function PromptInput() {
                 {suggestion.label}
               </BadgeButton>
             ))}
-          <MacRecommendationChip />
+          <MacRecommendationChip onSelect={seedPrompt} />
           <SystemDefaultsCTA />
           <HomebrewBadge />
         </div>
         <div className="ml-auto shrink-0">
-          <PromptHistoryBadge />
+          <PromptHistoryBadge onSelect={seedPrompt} />
         </div>
       </div>
     </div>