diff --git a/packages/cli/src/ui/components/StickyHeader.tsx b/packages/cli/src/ui/components/StickyHeader.tsx
index 62d5dcd22d..86546a1e71 100644
--- a/packages/cli/src/ui/components/StickyHeader.tsx
+++ b/packages/cli/src/ui/components/StickyHeader.tsx
@@ -26,7 +26,6 @@ export const StickyHeader: React.FC<StickyHeaderProps> = ({
   containerRef,
 }) => (
   <Box
-    ref={containerRef}
     sticky
     minHeight={1}
     flexShrink={0}
@@ -58,6 +57,7 @@ export const StickyHeader: React.FC<StickyHeaderProps> = ({
     }
   >
     <Box
+      ref={containerRef}
       borderStyle="round"
       width={width}
       borderColor={borderColor}
diff --git a/packages/cli/src/ui/components/messages/ShellToolMessage.tsx b/packages/cli/src/ui/components/messages/ShellToolMessage.tsx
index a7758c3390..b910661ebf 100644
--- a/packages/cli/src/ui/components/messages/ShellToolMessage.tsx
+++ b/packages/cli/src/ui/components/messages/ShellToolMessage.tsx
@@ -107,9 +107,9 @@ export const ShellToolMessage: React.FC<ShellToolMessageProps> = ({
     }
   };
 
-  useMouseClick(headerRef, handleFocus, { isActive: !!isThisShellFocusable });
+  useMouseClick(headerRef, handleFocus, { isActive: true });
 
-  useMouseClick(contentRef, handleFocus, { isActive: !!isThisShellFocusable });
+  useMouseClick(contentRef, handleFocus, { isActive: true });
 
   const { shouldShowFocusHint } = useFocusHint(
     isThisShellFocusable,
diff --git a/packages/cli/src/ui/components/messages/ToolShared.tsx b/packages/cli/src/ui/components/messages/ToolShared.tsx
index 4831e07279..fbd2024fa5 100644
--- a/packages/cli/src/ui/components/messages/ToolShared.tsx
+++ b/packages/cli/src/ui/components/messages/ToolShared.tsx
@@ -15,12 +15,12 @@ import {
   SHELL_FOCUS_HINT_DELAY_MS,
 } from '../../constants.js';
 import { theme } from '../../semantic-colors.js';
-import {
+import type {
+  CoreToolCallStatus,
   type Config,
   SHELL_TOOL_NAME,
   isCompletedAskUserTool,
-  type ToolResultDisplay,
-  CoreToolCallStatus,
+  type ToolResultDisplay
 } from '@google/gemini-cli-core';
 import { useInactivityTimer } from '../../hooks/useInactivityTimer.js';
 import { formatCommand } from '../../utils/keybindingUtils.js';
@@ -44,14 +44,10 @@ export function isShellTool(name: string): boolean {
  */
 export function isThisShellFocusable(
   name: string,
-  status: CoreToolCallStatus,
-  config?: Config,
+  _status: CoreToolCallStatus,
+  _config?: Config,
 ): boolean {
-  return !!(
-    isShellTool(name) &&
-    status === CoreToolCallStatus.Executing &&
-    config?.getEnableInteractiveShell()
-  );
+  return isShellTool(name);
 }
 
 /**
@@ -59,14 +55,13 @@ export function isThisShellFocusable(
  */
 export function isThisShellFocused(
   name: string,
-  status: CoreToolCallStatus,
+  _status: CoreToolCallStatus,
   ptyId?: number,
   activeShellPtyId?: number | null,
   embeddedShellFocused?: boolean,
 ): boolean {
   return !!(
     isShellTool(name) &&
-    status === CoreToolCallStatus.Executing &&
     ptyId === activeShellPtyId &&
     embeddedShellFocused
   );
diff --git a/packages/cli/src/ui/components/shared/Scrollable.tsx b/packages/cli/src/ui/components/shared/Scrollable.tsx
index ba6699254a..328ebd646f 100644
--- a/packages/cli/src/ui/components/shared/Scrollable.tsx
+++ b/packages/cli/src/ui/components/shared/Scrollable.tsx
@@ -5,12 +5,20 @@
  */
 
 import type React from 'react';
-import { useState, useRef, useCallback, useMemo, useLayoutEffect } from 'react';
-import { Box, ResizeObserver, type DOMElement } from 'ink';
+import {
+  useState,
+  useRef,
+  useCallback,
+  useMemo,
+  useLayoutEffect,
+  useEffect,
+} from 'react';
+import { Box, ResizeObserver, getBoundingBox, type DOMElement } from 'ink';
 import { useKeypress, type Key } from '../../hooks/useKeypress.js';
 import { useScrollable } from '../../contexts/ScrollProvider.js';
 import { useAnimatedScrollbar } from '../../hooks/useAnimatedScrollbar.js';
 import { useBatchedScroll } from '../../hooks/useBatchedScroll.js';
+import { useMouse, type MouseEvent } from '../../hooks/useMouse.js';
 import { keyMatchers, Command } from '../../keyMatchers.js';
 
 interface ScrollableProps {
@@ -115,13 +123,34 @@ export const Scrollable: React.FC<ScrollableProps> = ({
     [scrollToBottom],
   );
 
+  const [isHovered, setIsHovered] = useState(false);
+
+  useMouse(
+    (event: MouseEvent) => {
+      if (event.name === 'move' && viewportRef.current) {
+        const boundingBox = getBoundingBox(viewportRef.current);
+        if (boundingBox) {
+          const { x, y, width, height } = boundingBox;
+          const inside =
+            event.col >= x &&
+            event.col < x + width + 1 &&
+            event.row >= y &&
+            event.row < y + height;
+
+          if (inside !== isHovered) {
+            setIsHovered(inside);
+          }
+        }
+      }
+      return false;
+    },
+    { isActive: true },
+  );
+
   const { getScrollTop, setPendingScrollTop } = useBatchedScroll(scrollTop);
 
   const scrollBy = useCallback(
     (delta: number) => {
-      if (!hasFocus) {
-        return;
-      }
       const { scrollHeight, innerHeight } = sizeRef.current;
       const maxScroll = Math.max(0, scrollHeight - innerHeight);
       const current = Math.min(getScrollTop(), maxScroll);
@@ -132,14 +161,26 @@ export const Scrollable: React.FC<ScrollableProps> = ({
       setPendingScrollTop(next);
       setScrollTop(next);
     },
-    [getScrollTop, setPendingScrollTop, hasFocus],
+    [getScrollTop, setPendingScrollTop],
   );
 
   const { scrollbarColor, flashScrollbar, scrollByWithAnimation } =
     useAnimatedScrollbar(hasFocus, scrollBy);
 
+  // Flash scrollbar on hover for discoverability.
+  const wasHovered = useRef(isHovered);
+  useEffect(() => {
+    if (isHovered && !wasHovered.current && !hasFocus) {
+      flashScrollbar();
+    }
+    wasHovered.current = isHovered;
+  }, [isHovered, hasFocus, flashScrollbar]);
+
   useKeypress(
     (key: Key) => {
+      if (!hasFocus) {
+        return false;
+      }
       const { scrollHeight, innerHeight } = sizeRef.current;
       const scrollTop = getScrollTop();
       const maxScroll = Math.max(0, scrollHeight - innerHeight);
@@ -178,13 +219,20 @@ export const Scrollable: React.FC<ScrollableProps> = ({
   );
 
   const getScrollState = useCallback(() => {
+    if (!hasFocus && !isHovered) {
+      return {
+        scrollTop: 0,
+        scrollHeight: 0,
+        innerHeight: 0,
+      };
+    }
     const maxScroll = Math.max(0, size.scrollHeight - size.innerHeight);
     return {
       scrollTop: Math.min(getScrollTop(), maxScroll),
       scrollHeight: size.scrollHeight,
       innerHeight: size.innerHeight,
     };
-  }, [getScrollTop, size.scrollHeight, size.innerHeight]);
+  }, [hasFocus, isHovered, getScrollTop, size.scrollHeight, size.innerHeight]);
 
   const hasFocusCallback = useCallback(() => hasFocus, [hasFocus]);
 
@@ -209,11 +257,11 @@ export const Scrollable: React.FC<ScrollableProps> = ({
       width={width ?? maxWidth}
       height={height}
       flexDirection="column"
-      overflowY={hasFocus ? 'scroll' : 'hidden'}
+      overflowY={hasFocus || isHovered ? 'scroll' : 'hidden'}
       overflowX="hidden"
       scrollTop={scrollTop}
       flexGrow={flexGrow}
-      scrollbarThumbColor={hasFocus ? scrollbarColor : undefined}
+      scrollbarThumbColor={hasFocus || isHovered ? scrollbarColor : undefined}
     >
       {/*
         This inner box is necessary to prevent the parent from shrinking