diff --git a/src/pages/settings/Agents/DynamicAddAgentPage.tsx b/src/pages/settings/Agents/DynamicAddAgentPage.tsx
index 7254ad98bba4..e185049f7436 100644
--- a/src/pages/settings/Agents/DynamicAddAgentPage.tsx
+++ b/src/pages/settings/Agents/DynamicAddAgentPage.tsx
@@ -75,11 +75,12 @@ function DynamicAddAgentPageContent({route, template}: DynamicAddAgentPageConten
     const {windowWidth, windowHeight} = useWindowDimensions();
     const {isKeyboardActive} = useKeyboardState();
     const isInLandscapeMode = isInLandscapeModeUtil(windowWidth, windowHeight);
-    // On native portrait the prompt grows with its content up to a max height instead of filling the screen, so the open
+    // On native the prompt grows with its content up to a max height instead of filling the screen, so the open
     // keyboard can't squeeze it or hide the line being edited, and the form scrolls to fit it above the keyboard.
-    const shouldAutoGrowPromptInput = Platform.OS !== 'web' && !isInLandscapeMode;
+    const shouldAutoGrowPromptInput = Platform.OS !== 'web';
     const shouldUseScrollableLayout = shouldAutoGrowPromptInput || isInLandscapeMode;
     const shouldShrinkPromptInput = isInLandscapeMode && isKeyboardActive;
+    const landscapePromptHeight = shouldShrinkPromptInput ? PROMPT_MAX_HEIGHT_ON_KEYBOARD_OPEN_LANDSCAPE_MODE : styles.h42.height;
     const {accountID: currentUserAccountID, login: currentUserLogin, displayName} = useCurrentUserPersonalDetails();
     const defaultAgentName = template?.name ?? (displayName ? translate('addAgentPage.defaultAgentName', displayName) : undefined);
     const defaultPrompt = template?.prompt ?? translate('addAgentPage.defaultPrompt');
@@ -237,7 +238,11 @@ function DynamicAddAgentPageContent({route, template}: DynamicAddAgentPageConten
     };
 
     const promptTopOffsetRef = useRef(0);
-    const handleInputFocus = () => scrollToMultilineInput(formRef, shouldUseScrollableLayout, promptTopOffsetRef.current);
+    const isPromptFocusedRef = useRef(false);
+    const handleInputFocus = () => {
+        isPromptFocusedRef.current = true;
+        scrollToMultilineInput(formRef, shouldUseScrollableLayout, promptTopOffsetRef.current);
+    };
 
     const agentAvatar = avatarSource ? (
         <UserAvatar
@@ -309,13 +314,18 @@ function DynamicAddAgentPageContent({route, template}: DynamicAddAgentPageConten
                             </View>
                         )}
                         <View
-                            style={
-                                shouldShrinkPromptInput
-                                    ? StyleUtils.getHeight(PROMPT_MAX_HEIGHT_ON_KEYBOARD_OPEN_LANDSCAPE_MODE)
-                                    : [isInLandscapeMode && styles.h42, !isInLandscapeMode && !shouldAutoGrowPromptInput && styles.flex1]
-                            }
+                            style={[
+                                !shouldAutoGrowPromptInput &&
+                                    (shouldShrinkPromptInput
+                                        ? StyleUtils.getHeight(PROMPT_MAX_HEIGHT_ON_KEYBOARD_OPEN_LANDSCAPE_MODE)
+                                        : [isInLandscapeMode && styles.h42, !isInLandscapeMode && styles.flex1]),
+                            ]}
                             onLayout={(event) => {
                                 promptTopOffsetRef.current = event.nativeEvent.layout.y;
+                                // Rotation preserves focus, so reveal the prompt again after its new layout is measured.
+                                if (isPromptFocusedRef.current) {
+                                    scrollToMultilineInput(formRef, shouldUseScrollableLayout, promptTopOffsetRef.current);
+                                }
                             }}
                         >
                             <InputWrapper
@@ -329,12 +339,16 @@ function DynamicAddAgentPageContent({route, template}: DynamicAddAgentPageConten
                                 onKeyPress={submitFormOnModEnter}
                                 defaultValue={defaultPrompt}
                                 multiline
+                                // Keep native markdown sizing enabled across rotation so the input retains focus while its height limit changes.
                                 autoGrowHeight={shouldAutoGrowPromptInput}
-                                maxAutoGrowHeight={shouldAutoGrowPromptInput ? PROMPT_MAX_AUTO_GROW_HEIGHT : undefined}
+                                maxAutoGrowHeight={isInLandscapeMode ? landscapePromptHeight : PROMPT_MAX_AUTO_GROW_HEIGHT}
                                 containerStyles={shouldAutoGrowPromptInput ? undefined : [styles.h100]}
                                 touchableInputWrapperStyle={shouldAutoGrowPromptInput ? undefined : [styles.flex1]}
                                 inputStyle={[!shouldAutoGrowPromptInput && styles.flex1, styles.textAlignVerticalTop]}
                                 onFocus={handleInputFocus}
+                                onBlur={() => {
+                                    isPromptFocusedRef.current = false;
+                                }}
                             />
                         </View>
                         <Text style={[styles.textLabelSupporting]}>{`${translate('addAgentPage.copilotNote')} ${translate('workspace.rules.agentRules.disclaimer')}`}</Text>
diff --git a/src/pages/settings/Agents/Fields/DynamicEditPromptPage.tsx b/src/pages/settings/Agents/Fields/DynamicEditPromptPage.tsx
index b9f5506a9d2b..0ac450616c7d 100644
--- a/src/pages/settings/Agents/Fields/DynamicEditPromptPage.tsx
+++ b/src/pages/settings/Agents/Fields/DynamicEditPromptPage.tsx
@@ -42,16 +42,21 @@ function DynamicEditPromptPage({route}: DynamicEditPromptPageProps) {
     const styles = useThemeStyles();
     const {isKeyboardActive} = useKeyboardState();
     const isInLandscapeMode = useIsInLandscapeMode();
-    // On native portrait the prompt grows with its content up to a max height instead of filling the screen, so the open
+    // On native the prompt grows with its content up to a max height instead of filling the screen, so the open
     // keyboard can't squeeze it or hide the line being edited, and the form scrolls to fit it above the keyboard.
-    const shouldAutoGrowPromptInput = Platform.OS !== 'web' && !isInLandscapeMode;
+    const shouldAutoGrowPromptInput = Platform.OS !== 'web';
     const shouldUseScrollableLayout = shouldAutoGrowPromptInput || isInLandscapeMode;
     const shouldShrinkPromptInput = isInLandscapeMode && isKeyboardActive;
+    const landscapePromptHeight = shouldShrinkPromptInput ? PROMPT_MAX_HEIGHT_ON_KEYBOARD_OPEN_LANDSCAPE_MODE : styles.h42.height;
     const accountID = route.params.accountID;
     const [agentPrompt] = useOnyx(`${ONYXKEYS.COLLECTION.AGENT}${accountID}`);
     const formRef = useRef<FormRef>(null);
     const promptTopOffsetRef = useRef(0);
-    const scrollToInput = () => scrollToMultilineInput(formRef, shouldUseScrollableLayout, promptTopOffsetRef.current);
+    const isPromptFocusedRef = useRef(false);
+    const scrollToInput = () => {
+        isPromptFocusedRef.current = true;
+        scrollToMultilineInput(formRef, shouldUseScrollableLayout, promptTopOffsetRef.current);
+    };
     const backPath = useDynamicBackPath(DYNAMIC_ROUTES.AGENT_EDIT_PROMPT.path);
 
     const validate = (values: FormOnyxValues<typeof ONYXKEYS.FORMS.EDIT_AGENT_PROMPT_FORM>): FormInputErrors<typeof ONYXKEYS.FORMS.EDIT_AGENT_PROMPT_FORM> => {
@@ -116,13 +121,18 @@ function DynamicEditPromptPage({route}: DynamicEditPromptPageProps) {
             >
                 <View style={[styles.flex1, styles.flexColumn, styles.gap5]}>
                     <View
-                        style={
-                            shouldShrinkPromptInput
-                                ? StyleUtils.getHeight(PROMPT_MAX_HEIGHT_ON_KEYBOARD_OPEN_LANDSCAPE_MODE)
-                                : [isInLandscapeMode && styles.h42, !isInLandscapeMode && !shouldAutoGrowPromptInput && styles.flex1]
-                        }
+                        style={[
+                            !shouldAutoGrowPromptInput &&
+                                (shouldShrinkPromptInput
+                                    ? StyleUtils.getHeight(PROMPT_MAX_HEIGHT_ON_KEYBOARD_OPEN_LANDSCAPE_MODE)
+                                    : [isInLandscapeMode && styles.h42, !isInLandscapeMode && styles.flex1]),
+                        ]}
                         onLayout={(event) => {
                             promptTopOffsetRef.current = event.nativeEvent.layout.y;
+                            // Rotation preserves focus, so reveal the prompt again after its new layout is measured.
+                            if (isPromptFocusedRef.current) {
+                                scrollToMultilineInput(formRef, shouldUseScrollableLayout, promptTopOffsetRef.current);
+                            }
                         }}
                     >
                         <InputWrapper
@@ -135,12 +145,16 @@ function DynamicEditPromptPage({route}: DynamicEditPromptPageProps) {
                             excludedMarkdownStyles={['mentionReport']}
                             defaultValue={Str.htmlDecode(agentPrompt?.prompt ?? '')}
                             multiline
+                            // Keep native markdown sizing enabled across rotation so the input retains focus while its height limit changes.
                             autoGrowHeight={shouldAutoGrowPromptInput}
-                            maxAutoGrowHeight={shouldAutoGrowPromptInput ? PROMPT_MAX_AUTO_GROW_HEIGHT : undefined}
+                            maxAutoGrowHeight={isInLandscapeMode ? landscapePromptHeight : PROMPT_MAX_AUTO_GROW_HEIGHT}
                             containerStyles={shouldAutoGrowPromptInput ? undefined : [styles.h100]}
                             touchableInputWrapperStyle={shouldAutoGrowPromptInput ? undefined : [styles.flex1]}
                             inputStyle={[!shouldAutoGrowPromptInput && styles.flex1, styles.textAlignVerticalTop]}
                             onFocus={scrollToInput}
+                            onBlur={() => {
+                                isPromptFocusedRef.current = false;
+                            }}
                         />
                     </View>
                     <Text style={[styles.textMicroSupporting, styles.textAlignCenter]}>{translate('workspace.rules.agentRules.disclaimer')}</Text>
diff --git a/tests/unit/pages/settings/EditPromptPageTest.tsx b/tests/unit/pages/settings/EditPromptPageTest.tsx
index 4797947201c6..b127d6f166a0 100644
--- a/tests/unit/pages/settings/EditPromptPageTest.tsx
+++ b/tests/unit/pages/settings/EditPromptPageTest.tsx
@@ -1,19 +1,29 @@
-import {render} from '@testing-library/react-native';
+import {act, fireEvent, render} from '@testing-library/react-native';
 
+import useIsInLandscapeMode from '@hooks/useIsInLandscapeMode';
 import useOnyx from '@hooks/useOnyx';
 
 import type {PlatformStackScreenProps} from '@libs/Navigation/PlatformStackNavigation/types';
 import type {SettingsNavigatorParamList} from '@libs/Navigation/types';
 
 import EditPromptPage from '@pages/settings/Agents/Fields/DynamicEditPromptPage';
+import scrollToMultilineInput from '@pages/settings/Agents/scrollToMultilineInput';
 
 import ONYXKEYS from '@src/ONYXKEYS';
 import type SCREENS from '@src/SCREENS';
 
 import React from 'react';
+import {Platform, View} from 'react-native';
 
 import createMock from '../../../utils/createMock';
 
+const mockPromptMount = jest.fn();
+const mockPromptProps = jest.fn<void, [{onFocus?: () => void; onBlur?: () => void}]>();
+
+jest.mock('@pages/settings/Agents/scrollToMultilineInput', () => jest.fn());
+
+jest.mock('@hooks/useIsInLandscapeMode', () => jest.fn(() => false));
+
 jest.mock('@userActions/Agent', () => ({
     updateAgentPrompt: jest.fn(),
 }));
@@ -76,7 +86,12 @@ jest.mock('@components/Form/FormProvider', () => {
 });
 
 jest.mock('@components/Form/InputWrapper', () => {
-    function MockInputWrapper({inputID, defaultValue}: {inputID: string; defaultValue?: string}) {
+    const {useEffect} = jest.requireActual<typeof React>('react');
+    function MockInputWrapper({inputID, defaultValue, ...props}: {inputID: string; defaultValue?: string; onFocus?: () => void; onBlur?: () => void}) {
+        mockPromptProps(props);
+        useEffect(() => {
+            mockPromptMount();
+        }, []);
         return `${inputID}::${defaultValue ?? ''}`;
     }
     return MockInputWrapper;
@@ -98,6 +113,66 @@ describe('EditPromptPage', () => {
         mockUseOnyx.mockReturnValue([undefined, {status: 'loaded'}]);
     });
 
+    it('keeps the prompt mounted when rotating on native', () => {
+        // Given a native prompt editor in portrait, remounting would discard the input's focus and selection.
+        const platform = jest.replaceProperty(Platform, 'OS', 'ios');
+        const mockLandscape = jest.mocked(useIsInLandscapeMode);
+        mockLandscape.mockReturnValue(false);
+        const page = (
+            <EditPromptPage
+                route={mockRoute}
+                navigation={mockNavigation}
+            />
+        );
+        const {rerender} = render(page);
+        expect(mockPromptMount).toHaveBeenCalledTimes(1);
+
+        // When the device rotates to landscape and back while the editor is open.
+        mockLandscape.mockReturnValue(true);
+        rerender(React.cloneElement(page));
+        mockLandscape.mockReturnValue(false);
+        rerender(React.cloneElement(page));
+
+        // Then the original input survives both layout changes, preserving native editing state.
+        expect(mockPromptMount).toHaveBeenCalledTimes(1);
+        platform.restore();
+    });
+
+    it('reveals the focused prompt after rotation changes its layout', () => {
+        // Given an iOS prompt that is being edited, focus will survive rotation.
+        const platform = jest.replaceProperty(Platform, 'OS', 'ios');
+        const {UNSAFE_getAllByType: getAllByType} = render(
+            <EditPromptPage
+                route={mockRoute}
+                navigation={mockNavigation}
+            />,
+        );
+        act(() => mockPromptProps.mock.lastCall?.[0].onFocus?.());
+        jest.mocked(scrollToMultilineInput).mockClear();
+        const promptContainer = getAllByType(View).find((view) => {
+            const child: unknown = view.props.children;
+            return React.isValidElement<{inputID?: string}>(child) && child.props.inputID === 'prompt';
+        });
+        if (!promptContainer) {
+            throw new Error('Prompt container not found');
+        }
+
+        // When rotation moves the still-focused field, the updated offset must be used without another focus event.
+        fireEvent(promptContainer, 'layout', {nativeEvent: {layout: {x: 0, y: 120, width: 600, height: 76}}});
+
+        // Then the field is revealed using the newly measured position.
+        expect(scrollToMultilineInput).toHaveBeenLastCalledWith(expect.anything(), true, 120);
+
+        // When editing ends, later layout changes should preserve the user's scroll position.
+        act(() => mockPromptProps.mock.lastCall?.[0].onBlur?.());
+        jest.mocked(scrollToMultilineInput).mockClear();
+        fireEvent(promptContainer, 'layout', {nativeEvent: {layout: {x: 0, y: 180, width: 300, height: 200}}});
+
+        // Then the page does not scroll to an unfocused field.
+        expect(scrollToMultilineInput).not.toHaveBeenCalled();
+        platform.restore();
+    });
+
     it('renders page title', () => {
         const {toJSON} = render(
             <EditPromptPage