diff --git a/src/pages/settings/Profile/AgentAIPromptSection.tsx b/src/pages/settings/Profile/AgentAIPromptSection.tsx
index dc8a219300a3..f71a4201bfdb 100644
--- a/src/pages/settings/Profile/AgentAIPromptSection.tsx
+++ b/src/pages/settings/Profile/AgentAIPromptSection.tsx
@@ -5,12 +5,14 @@ import type {RefObject} from 'react';
 import type {ScrollView as RNScrollView, TextInputKeyPressEvent} from 'react-native';
 import {Keyboard} from 'react-native';
 import Button from '@components/Button';
+import ErrorMessageRow from '@components/ErrorMessageRow';
 import OfflineWithFeedback from '@components/OfflineWithFeedback';
 import Section from '@components/Section';
 import TextInput from '@components/TextInput';
 import type {BaseTextInputRef} from '@components/TextInput/BaseTextInput/types';
 import {useMemoizedLazyExpensifyIcons} from '@hooks/useLazyAsset';
 import useLocalize from '@hooks/useLocalize';
+import useNetwork from '@hooks/useNetwork';
 import useOnyx from '@hooks/useOnyx';
 import useThemeStyles from '@hooks/useThemeStyles';
 import {clearAgentPromptUpdateError, openProfilePage, updateAgentPrompt} from '@libs/actions/Agent';
@@ -47,6 +49,7 @@ function scrollInputIntoView(parentScrollViewRef: RefObject<RNScrollView | null>
 
 function AgentAIPromptSection({accountID, parentScrollViewRef}: AgentAIPromptSectionProps) {
     const {translate} = useLocalize();
+    const {isOffline} = useNetwork();
     const styles = useThemeStyles();
     const icons = useMemoizedLazyExpensifyIcons(['Checkmark']);
     const [agentPrompt] = useOnyx(`${ONYXKEYS.COLLECTION.SHARED_NVP_AGENT_PROMPT}${accountID}`);
@@ -95,19 +98,23 @@ function AgentAIPromptSection({accountID, parentScrollViewRef}: AgentAIPromptSec
         // eslint-disable-next-line react-hooks/exhaustive-deps
     }, [agentPrompt?.promptErrors]);
 
+    const triggerSavedConfirmation = useCallback(() => {
+        setShowSavedConfirmation(true);
+        if (savedConfirmationTimerRef.current) {
+            clearTimeout(savedConfirmationTimerRef.current);
+        }
+        savedConfirmationTimerRef.current = setTimeout(() => {
+            setShowSavedConfirmation(false);
+            savedConfirmationTimerRef.current = null;
+        }, SAVED_CONFIRMATION_DURATION_MS);
+    }, []);
+
     useEffect(() => {
         if (wasSavingRef.current && !isSaving && !hasPromptErrors) {
-            setShowSavedConfirmation(true);
-            if (savedConfirmationTimerRef.current) {
-                clearTimeout(savedConfirmationTimerRef.current);
-            }
-            savedConfirmationTimerRef.current = setTimeout(() => {
-                setShowSavedConfirmation(false);
-                savedConfirmationTimerRef.current = null;
-            }, SAVED_CONFIRMATION_DURATION_MS);
+            triggerSavedConfirmation();
         }
         wasSavingRef.current = isSaving;
-    }, [isSaving, hasPromptErrors]);
+    }, [isSaving, hasPromptErrors, triggerSavedConfirmation]);
 
     useEffect(() => {
         return () => {
@@ -131,7 +138,7 @@ function AgentAIPromptSection({accountID, parentScrollViewRef}: AgentAIPromptSec
     }, [parentScrollViewRef]);
 
     const handleSave = () => {
-        if (isSaving) {
+        if (isSaving && !isOffline) {
             return;
         }
 
@@ -147,6 +154,12 @@ function AgentAIPromptSection({accountID, parentScrollViewRef}: AgentAIPromptSec
         }
         dismissInput();
         updateAgentPrompt(accountID, trimmed, agentPrompt?.prompt ?? '');
+
+        // Offline: treat the optimistic write as the final state for UX purposes. The request will be
+        // replayed on reconnect, so showing "Saved" immediately matches the queued-but-done intent.
+        if (isOffline) {
+            triggerSavedConfirmation();
+        }
     };
 
     const handleChangeText = (text: string) => {
@@ -172,11 +185,7 @@ function AgentAIPromptSection({accountID, parentScrollViewRef}: AgentAIPromptSec
             childrenStyles={styles.pt5}
             titleStyles={styles.accountSettingsSectionTitle}
         >
-            <OfflineWithFeedback
-                errors={agentPrompt?.promptErrors}
-                pendingAction={agentPrompt?.pendingAction}
-                onClose={() => clearAgentPromptUpdateError(accountID)}
-            >
+            <OfflineWithFeedback pendingAction={agentPrompt?.pendingAction}>
                 <TextInput
                     ref={inputRef}
                     label={translate('profilePage.aiPromptSection.prompt')}
@@ -188,7 +197,7 @@ function AgentAIPromptSection({accountID, parentScrollViewRef}: AgentAIPromptSec
                     autoGrowHeight
                     maxAutoGrowHeight={variables.lineHeightNormal * MAX_VISIBLE_PROMPT_LINES}
                     errorText={errorText}
-                    containerStyles={[styles.mb4]}
+                    containerStyles={[styles.mb3]}
                     testID="ai-prompt-input"
                     onFocus={handleInputFocus}
                 />
@@ -198,11 +207,16 @@ function AgentAIPromptSection({accountID, parentScrollViewRef}: AgentAIPromptSec
                 text={showSavedConfirmation ? translate('profilePage.aiPromptSection.saved') : translate('common.save')}
                 icon={showSavedConfirmation ? icons.Checkmark : undefined}
                 onPress={handleSave}
-                isLoading={isSaving}
-                isDisabled={hasHtmlTag || isSaving}
+                isLoading={isSaving && !isOffline}
+                isDisabled={hasHtmlTag || (isSaving && !isOffline)}
                 style={[styles.alignSelfStart]}
                 testID="save-prompt-button"
             />
+            <ErrorMessageRow
+                errors={agentPrompt?.promptErrors}
+                errorRowStyles={[styles.mt3]}
+                onDismiss={() => clearAgentPromptUpdateError(accountID)}
+            />
         </Section>
     );
 }
diff --git a/tests/ui/ProfilePageTest.tsx b/tests/ui/ProfilePageTest.tsx
index 304d0ffb6d7c..9a9b8bbd6c38 100644
--- a/tests/ui/ProfilePageTest.tsx
+++ b/tests/ui/ProfilePageTest.tsx
@@ -343,6 +343,32 @@ describe('ProfilePage - agent account', () => {
         expect(saveButtonProps.accessibilityState?.disabled).toBe(true);
     });
 
+    it('allows re-saving an edited prompt while offline even when a previous save is still pending', async () => {
+        const accountID = 123;
+        const mockUpdateAgentPrompt = jest.mocked(AgentActions.updateAgentPrompt);
+        await setupUser('agent_123@expensify.ai');
+
+        await act(async () => {
+            // Simulate a first offline save that is queued but not yet replayed: pendingAction stays 'update',
+            // so isSaving is true. The button is intentionally not disabled while offline.
+            await Onyx.merge(`${ONYXKEYS.COLLECTION.SHARED_NVP_AGENT_PROMPT}${accountID}`, {
+                prompt: 'First offline edit.',
+                pendingAction: 'update',
+            });
+            await Onyx.merge(ONYXKEYS.NETWORK, {shouldForceOffline: true});
+        });
+        await waitForBatchedUpdatesWithAct();
+
+        renderPageWithNavigation(SCREENS.SETTINGS.PROFILE.ROOT);
+        await waitForBatchedUpdatesWithAct();
+
+        fireEvent.changeText(screen.getByTestId('ai-prompt-input'), 'Second offline edit.');
+        fireEvent.press(screen.getByTestId('save-prompt-button'));
+        await waitForBatchedUpdatesWithAct();
+
+        expect(mockUpdateAgentPrompt).toHaveBeenCalledWith(accountID, 'Second offline edit.', 'First offline edit.');
+    });
+
     it('does not call updateAgentPrompt when saving blank prompt', async () => {
         const accountID = 123;
         const mockUpdateAgentPrompt = jest.mocked(AgentActions.updateAgentPrompt);