diff --git a/src/core/webview/webviewMessageHandler.ts b/src/core/webview/webviewMessageHandler.ts
index 673f1bc17b..a4d9dafecf 100644
--- a/src/core/webview/webviewMessageHandler.ts
+++ b/src/core/webview/webviewMessageHandler.ts
@@ -829,13 +829,12 @@ export const webviewMessageHandler = async (
 			break
 		case "updateSupportPrompt":
 			try {
-				if (Object.keys(message?.values ?? {}).length === 0) {
+				if (!message?.values) {
 					return
 				}
 
-				const existingPrompts = getGlobalState("customSupportPrompts") ?? {}
-				const updatedPrompts = { ...existingPrompts, ...message.values }
-				await updateGlobalState("customSupportPrompts", updatedPrompts)
+				// Replace all prompts with the new values from the cached state
+				await updateGlobalState("customSupportPrompts", message.values)
 				await provider.postStateToWebview()
 			} catch (error) {
 				provider.log(
@@ -844,24 +843,6 @@ export const webviewMessageHandler = async (
 				vscode.window.showErrorMessage(t("common:errors.update_support_prompt"))
 			}
 			break
-		case "resetSupportPrompt":
-			try {
-				if (!message?.text) {
-					return
-				}
-
-				const existingPrompts = getGlobalState("customSupportPrompts") ?? {}
-				const updatedPrompts = { ...existingPrompts }
-				updatedPrompts[message.text] = undefined
-				await updateGlobalState("customSupportPrompts", updatedPrompts)
-				await provider.postStateToWebview()
-			} catch (error) {
-				provider.log(
-					`Error reset support prompt: ${JSON.stringify(error, Object.getOwnPropertyNames(error), 2)}`,
-				)
-				vscode.window.showErrorMessage(t("common:errors.reset_support_prompt"))
-			}
-			break
 		case "updatePrompt":
 			if (message.promptMode && message.customPrompt !== undefined) {
 				const existingPrompts = getGlobalState("customModePrompts") ?? {}
diff --git a/src/shared/WebviewMessage.ts b/src/shared/WebviewMessage.ts
index 7574959e14..5186c716b9 100644
--- a/src/shared/WebviewMessage.ts
+++ b/src/shared/WebviewMessage.ts
@@ -118,7 +118,6 @@ export interface WebviewMessage {
 		| "mode"
 		| "updatePrompt"
 		| "updateSupportPrompt"
-		| "resetSupportPrompt"
 		| "getSystemPrompt"
 		| "copySystemPrompt"
 		| "systemPrompt"
diff --git a/webview-ui/src/components/settings/PromptsSettings.tsx b/webview-ui/src/components/settings/PromptsSettings.tsx
index ffeffca8ea..568b8eeee1 100644
--- a/webview-ui/src/components/settings/PromptsSettings.tsx
+++ b/webview-ui/src/components/settings/PromptsSettings.tsx
@@ -11,11 +11,14 @@ import { SectionHeader } from "./SectionHeader"
 import { Section } from "./Section"
 import { MessageSquare } from "lucide-react"
 
-const PromptsSettings = () => {
-	const { t } = useAppTranslation()
+interface PromptsSettingsProps {
+	customSupportPrompts: Record<string, string | undefined>
+	setCustomSupportPrompts: (prompts: Record<string, string | undefined>) => void
+}
 
-	const { customSupportPrompts, listApiConfigMeta, enhancementApiConfigId, setEnhancementApiConfigId } =
-		useExtensionState()
+const PromptsSettings = ({ customSupportPrompts, setCustomSupportPrompts }: PromptsSettingsProps) => {
+	const { t } = useAppTranslation()
+	const { listApiConfigMeta, enhancementApiConfigId, setEnhancementApiConfigId } = useExtensionState()
 
 	const [testPrompt, setTestPrompt] = useState("")
 	const [isEnhancing, setIsEnhancing] = useState(false)
@@ -37,19 +40,14 @@ const PromptsSettings = () => {
 	}, [])
 
 	const updateSupportPrompt = (type: SupportPromptType, value: string | undefined) => {
-		vscode.postMessage({
-			type: "updateSupportPrompt",
-			values: {
-				[type]: value,
-			},
-		})
+		const updatedPrompts = { ...customSupportPrompts, [type]: value }
+		setCustomSupportPrompts(updatedPrompts)
 	}
 
 	const handleSupportReset = (type: SupportPromptType) => {
-		vscode.postMessage({
-			type: "resetSupportPrompt",
-			text: type,
-		})
+		const updatedPrompts = { ...customSupportPrompts }
+		delete updatedPrompts[type]
+		setCustomSupportPrompts(updatedPrompts)
 	}
 
 	const getSupportPromptValue = (type: SupportPromptType): string => {
diff --git a/webview-ui/src/components/settings/SettingsView.tsx b/webview-ui/src/components/settings/SettingsView.tsx
index aea9457994..5a330c8996 100644
--- a/webview-ui/src/components/settings/SettingsView.tsx
+++ b/webview-ui/src/components/settings/SettingsView.tsx
@@ -171,6 +171,7 @@ const SettingsView = forwardRef<SettingsViewRef, SettingsViewProps>(({ onDone, t
 		customCondensingPrompt,
 		codebaseIndexConfig,
 		codebaseIndexModels,
+		customSupportPrompts,
 	} = cachedState
 
 	const apiConfiguration = useMemo(() => cachedState.apiConfiguration ?? {}, [cachedState.apiConfiguration])
@@ -242,6 +243,17 @@ const SettingsView = forwardRef<SettingsViewRef, SettingsViewProps>(({ onDone, t
 		})
 	}, [])
 
+	const setCustomSupportPromptsField = useCallback((prompts: Record<string, string | undefined>) => {
+		setCachedState((prevState) => {
+			if (JSON.stringify(prevState.customSupportPrompts) === JSON.stringify(prompts)) {
+				return prevState
+			}
+
+			setChangeDetected(true)
+			return { ...prevState, customSupportPrompts: prompts }
+		})
+	}, [])
+
 	const isSettingValid = !errorMessage
 
 	const handleSubmit = () => {
@@ -299,6 +311,7 @@ const SettingsView = forwardRef<SettingsViewRef, SettingsViewProps>(({ onDone, t
 			vscode.postMessage({ type: "alwaysAllowSubtasks", bool: alwaysAllowSubtasks })
 			vscode.postMessage({ type: "condensingApiConfigId", text: condensingApiConfigId || "" })
 			vscode.postMessage({ type: "updateCondensingPrompt", text: customCondensingPrompt || "" })
+			vscode.postMessage({ type: "updateSupportPrompt", values: customSupportPrompts || {} })
 			vscode.postMessage({ type: "upsertApiConfiguration", text: currentApiConfigName, apiConfiguration })
 			vscode.postMessage({ type: "telemetrySetting", text: telemetrySetting })
 			vscode.postMessage({ type: "codebaseIndexConfig", values: codebaseIndexConfig })
@@ -653,7 +666,12 @@ const SettingsView = forwardRef<SettingsViewRef, SettingsViewProps>(({ onDone, t
 					)}
 
 					{/* Prompts Section */}
-					{activeTab === "prompts" && <PromptsSettings />}
+					{activeTab === "prompts" && (
+						<PromptsSettings
+							customSupportPrompts={customSupportPrompts || {}}
+							setCustomSupportPrompts={setCustomSupportPromptsField}
+						/>
+					)}
 
 					{/* Experimental Section */}
 					{activeTab === "experimental" && (
diff --git a/webview-ui/src/context/ExtensionStateContext.tsx b/webview-ui/src/context/ExtensionStateContext.tsx
index e15c247603..ab79f63df8 100644
--- a/webview-ui/src/context/ExtensionStateContext.tsx
+++ b/webview-ui/src/context/ExtensionStateContext.tsx
@@ -123,29 +123,22 @@ export interface ExtensionStateContextType extends ExtensionState {
 export const ExtensionStateContext = createContext<ExtensionStateContextType | undefined>(undefined)
 
 export const mergeExtensionState = (prevState: ExtensionState, newState: ExtensionState) => {
-	const {
-		customModePrompts: prevCustomModePrompts,
-		customSupportPrompts: prevCustomSupportPrompts,
-		experiments: prevExperiments,
-		...prevRest
-	} = prevState
+	const { customModePrompts: prevCustomModePrompts, experiments: prevExperiments, ...prevRest } = prevState
 
 	const {
 		apiConfiguration,
 		customModePrompts: newCustomModePrompts,
-		customSupportPrompts: newCustomSupportPrompts,
+		customSupportPrompts,
 		experiments: newExperiments,
 		...newRest
 	} = newState
 
 	const customModePrompts = { ...prevCustomModePrompts, ...newCustomModePrompts }
-	const customSupportPrompts = { ...prevCustomSupportPrompts, ...newCustomSupportPrompts }
 	const experiments = { ...prevExperiments, ...newExperiments }
 	const rest = { ...prevRest, ...newRest }
 
-	// Note that we completely replace the previous apiConfiguration object with
-	// a new one since the state that is broadcast is the entire apiConfiguration
-	// and therefore merging is not necessary.
+	// Note that we completely replace the previous apiConfiguration and customSupportPrompts objects
+	// with new ones since the state that is broadcast is the entire objects so merging is not necessary.
 	return { ...rest, apiConfiguration, customModePrompts, customSupportPrompts, experiments }
 }