diff --git a/packages/cli/src/ui/App.test.tsx b/packages/cli/src/ui/App.test.tsx
index 1a8851685a..695de98684 100644
--- a/packages/cli/src/ui/App.test.tsx
+++ b/packages/cli/src/ui/App.test.tsx
@@ -16,6 +16,21 @@ import { AppContext, type AppState } from './contexts/AppContext.js';
 import { SettingsContext } from './contexts/SettingsContext.js';
 import { LoadedSettings, type SettingsFile } from '../config/settings.js';
 
+// Mock the ResizeObserver API for tests.
+class ResizeObserver {
+  observe() {
+    // do nothing
+  }
+  unobserve() {
+    // do nothing
+  }
+  disconnect() {
+    // do nothing
+  }
+}
+
+global.ResizeObserver = ResizeObserver;
+
 vi.mock('ink', async (importOriginal) => {
   const original = await importOriginal<typeof import('ink')>();
   return {
diff --git a/packages/cli/src/ui/components/MainContent.test.tsx b/packages/cli/src/ui/components/MainContent.test.tsx
index 63cbdce790..b0160db814 100644
--- a/packages/cli/src/ui/components/MainContent.test.tsx
+++ b/packages/cli/src/ui/components/MainContent.test.tsx
@@ -95,7 +95,7 @@ describe('MainContent', () => {
   });
 
   it('renders in normal buffer mode', async () => {
-    const { lastFrame } = render(<MainContent />);
+    const { lastFrame } = render(<MainContent composerHeight={0} />);
     await waitFor(() => expect(lastFrame()).toContain('AppHeader'));
     const output = lastFrame();
 
@@ -105,7 +105,7 @@ describe('MainContent', () => {
 
   it('renders in alternate buffer mode', async () => {
     vi.mocked(useAlternateBuffer).mockReturnValue(true);
-    const { lastFrame } = render(<MainContent />);
+    const { lastFrame } = render(<MainContent composerHeight={0} />);
     await waitFor(() => expect(lastFrame()).toContain('ScrollableList'));
     const output = lastFrame();
 
@@ -116,7 +116,7 @@ describe('MainContent', () => {
 
   it('does not constrain height in alternate buffer mode', async () => {
     vi.mocked(useAlternateBuffer).mockReturnValue(true);
-    const { lastFrame } = render(<MainContent />);
+    const { lastFrame } = render(<MainContent composerHeight={0} />);
     await waitFor(() => expect(lastFrame()).toContain('HistoryItem: Hello'));
     const output = lastFrame();
 
diff --git a/packages/cli/src/ui/components/MainContent.tsx b/packages/cli/src/ui/components/MainContent.tsx
index 7f3982eec0..2a60109613 100644
--- a/packages/cli/src/ui/components/MainContent.tsx
+++ b/packages/cli/src/ui/components/MainContent.tsx
@@ -16,15 +16,20 @@ import { SCROLL_TO_ITEM_END } from './shared/VirtualizedList.js';
 import { ScrollableList } from './shared/ScrollableList.js';
 import { useMemo, memo, useCallback } from 'react';
 import { MAX_GEMINI_MESSAGE_LINES } from '../constants.js';
+import { MaxSizedBox } from './shared/MaxSizedBox.js';
 
 const MemoizedHistoryItemDisplay = memo(HistoryItemDisplay);
 const MemoizedAppHeader = memo(AppHeader);
 
+interface MainContentProps {
+  composerHeight: number;
+}
+
 // Limit Gemini messages to a very high number of lines to mitigate performance
 // issues in the worst case if we somehow get an enormous response from Gemini.
 // This threshold is arbitrary but should be high enough to never impact normal
 // usage.
-export const MainContent = () => {
+export const MainContent = ({ composerHeight }: MainContentProps) => {
   const { version } = useAppContext();
   const uiState = useUIState();
   const isAlternateBuffer = useAlternateBuffer();
@@ -144,17 +149,26 @@ export const MainContent = () => {
   }
 
   return (
-    <>
-      <Static
-        key={uiState.historyRemountKey}
-        items={[
-          <AppHeader key="app-header" version={version} />,
-          ...historyItems,
-        ]}
+    <Box flexGrow={1} flexShrink={1} flexDirection="column" overflow="hidden">
+      <MaxSizedBox
+        maxHeight={
+          availableTerminalHeight
+            ? availableTerminalHeight - composerHeight
+            : // HACK: Sometimes availableTerminalHeight is 0 on the first render.
+              1
+        }
       >
-        {(item) => item}
-      </Static>
-      {pendingItems}
-    </>
+        <Static
+          key={uiState.historyRemountKey}
+          items={[
+            <AppHeader key="app-header" version={version} />,
+            ...historyItems,
+          ]}
+        >
+          {(item) => item}
+        </Static>
+        {pendingItems}
+      </MaxSizedBox>
+    </Box>
   );
 };
diff --git a/packages/cli/src/ui/layouts/DefaultAppLayout.tsx b/packages/cli/src/ui/layouts/DefaultAppLayout.tsx
index bf68aee85d..5bfc0628b0 100644
--- a/packages/cli/src/ui/layouts/DefaultAppLayout.tsx
+++ b/packages/cli/src/ui/layouts/DefaultAppLayout.tsx
@@ -4,8 +4,7 @@
  * SPDX-License-Identifier: Apache-2.0
  */
 
-import type React from 'react';
-import { Box } from 'ink';
+import { type DOMElement, Box } from 'ink';
 import { Notifications } from '../components/Notifications.js';
 import { MainContent } from '../components/MainContent.js';
 import { DialogManager } from '../components/DialogManager.js';
@@ -15,10 +14,36 @@ import { useUIState } from '../contexts/UIStateContext.js';
 import { useFlickerDetector } from '../hooks/useFlickerDetector.js';
 import { useAlternateBuffer } from '../hooks/useAlternateBuffer.js';
 import { CopyModeWarning } from '../components/CopyModeWarning.js';
+import { useState, useRef, useCallback } from 'react';
 
 export const DefaultAppLayout: React.FC = () => {
   const uiState = useUIState();
   const isAlternateBuffer = useAlternateBuffer();
+  const [composerHeight, setComposerHeight] = useState(0);
+  const observerRef = useRef<ResizeObserver | null>(null);
+
+  const onRefChange = useCallback(
+    (node: DOMElement | null) => {
+      if (observerRef.current) {
+        observerRef.current.disconnect();
+        observerRef.current = null;
+      }
+
+      uiState.mainControlsRef.current = node;
+
+      if (node && typeof ResizeObserver !== 'undefined') {
+        const observer = new ResizeObserver((entries) => {
+          const entry = entries[0];
+          if (entry) {
+            setComposerHeight(entry.contentRect.height);
+          }
+        });
+        observer.observe(node as unknown as Element);
+        observerRef.current = observer;
+      }
+    },
+    [uiState.mainControlsRef],
+  );
 
   const { rootUiRef, terminalHeight } = uiState;
   useFlickerDetector(rootUiRef, terminalHeight);
@@ -37,14 +62,9 @@ export const DefaultAppLayout: React.FC = () => {
       overflow="hidden"
       ref={uiState.rootUiRef}
     >
-      <MainContent />
+      <MainContent composerHeight={composerHeight} />
 
-      <Box
-        flexDirection="column"
-        ref={uiState.mainControlsRef}
-        flexShrink={0}
-        flexGrow={0}
-      >
+      <Box flexDirection="column" ref={onRefChange} flexShrink={0} flexGrow={0}>
         <Notifications />
         <CopyModeWarning />
 
diff --git a/packages/cli/src/ui/layouts/ScreenReaderAppLayout.tsx b/packages/cli/src/ui/layouts/ScreenReaderAppLayout.tsx
index d88f3f1fb2..95df0ab633 100644
--- a/packages/cli/src/ui/layouts/ScreenReaderAppLayout.tsx
+++ b/packages/cli/src/ui/layouts/ScreenReaderAppLayout.tsx
@@ -30,7 +30,7 @@ export const ScreenReaderAppLayout: React.FC = () => {
       <Notifications />
       <Footer />
       <Box flexGrow={1} overflow="hidden">
-        <MainContent />
+        <MainContent composerHeight={0} />
       </Box>
       {uiState.dialogsVisible ? (
         <DialogManager
diff --git a/packages/cli/test-setup.ts b/packages/cli/test-setup.ts
index 67c997c0fc..7f5aa4481b 100644
--- a/packages/cli/test-setup.ts
+++ b/packages/cli/test-setup.ts
@@ -4,6 +4,24 @@
  * SPDX-License-Identifier: Apache-2.0
  */
 
+// Mock the ResizeObserver API for tests.
+// This needs to be at the top of the file to ensure it's available globally
+// before any other modules (especially React components) are imported.
+// Otherwise, we can get a "ResizeObserver is not defined" error during test runs.
+class ResizeObserver {
+  observe() {
+    // do nothing
+  }
+  unobserve() {
+    // do nothing
+  }
+  disconnect() {
+    // do nothing
+  }
+}
+
+global.ResizeObserver = ResizeObserver;
+
 import { vi, beforeEach, afterEach } from 'vitest';
 import { format } from 'node:util';