diff --git a/webview-ui/src/components/chat/ChatTextArea.tsx b/webview-ui/src/components/chat/ChatTextArea.tsx
index a38b4538d05..7b404ddccb6 100644
--- a/webview-ui/src/components/chat/ChatTextArea.tsx
+++ b/webview-ui/src/components/chat/ChatTextArea.tsx
@@ -115,8 +115,25 @@ const ChatTextArea = forwardRef<HTMLTextAreaElement, ChatTextAreaProps>(
 				const message = event.data
 
 				if (message.type === "enhancedPrompt") {
-					if (message.text) {
-						setInputValue(message.text)
+					if (message.text && textAreaRef.current) {
+						try {
+							// Use execCommand to replace text while preserving undo history
+							if (document.execCommand) {
+								// Use native browser methods to preserve undo stack
+								const textarea = textAreaRef.current
+
+								// Focus the textarea to ensure it's the active element
+								textarea.focus()
+
+								// Select all text first
+								textarea.select()
+								document.execCommand("insertText", false, message.text)
+							} else {
+								setInputValue(message.text)
+							}
+						} catch {
+							setInputValue(message.text)
+						}
 					}
 
 					setIsEnhancingPrompt(false)
diff --git a/webview-ui/src/components/chat/__tests__/ChatTextArea.spec.tsx b/webview-ui/src/components/chat/__tests__/ChatTextArea.spec.tsx
index 75324c97f4b..973420207c7 100644
--- a/webview-ui/src/components/chat/__tests__/ChatTextArea.spec.tsx
+++ b/webview-ui/src/components/chat/__tests__/ChatTextArea.spec.tsx
@@ -184,10 +184,27 @@ describe("ChatTextArea", () => {
 	})
 
 	describe("enhanced prompt response", () => {
-		it("should update input value when receiving enhanced prompt", () => {
+		it("should update input value using native browser methods when receiving enhanced prompt", () => {
 			const setInputValue = vi.fn()
 
-			render(<ChatTextArea {...defaultProps} setInputValue={setInputValue} />)
+			// Mock document.execCommand
+			const mockExecCommand = vi.fn().mockReturnValue(true)
+			Object.defineProperty(document, "execCommand", {
+				value: mockExecCommand,
+				writable: true,
+			})
+
+			const { container } = render(
+				<ChatTextArea {...defaultProps} setInputValue={setInputValue} inputValue="Original prompt" />,
+			)
+
+			const textarea = container.querySelector("textarea")!
+
+			// Mock textarea methods
+			const mockSelect = vi.fn()
+			const mockFocus = vi.fn()
+			textarea.select = mockSelect
+			textarea.focus = mockFocus
 
 			// Simulate receiving enhanced prompt message
 			window.dispatchEvent(
@@ -199,8 +216,54 @@ describe("ChatTextArea", () => {
 				}),
 			)
 
+			// Verify native browser methods were used
+			expect(mockFocus).toHaveBeenCalled()
+			expect(mockSelect).toHaveBeenCalled()
+			expect(mockExecCommand).toHaveBeenCalledWith("insertText", false, "Enhanced test prompt")
+		})
+
+		it("should fallback to setInputValue when execCommand is not available", () => {
+			const setInputValue = vi.fn()
+
+			// Mock document.execCommand to be undefined (not available)
+			Object.defineProperty(document, "execCommand", {
+				value: undefined,
+				writable: true,
+			})
+
+			render(<ChatTextArea {...defaultProps} setInputValue={setInputValue} inputValue="Original prompt" />)
+
+			// Simulate receiving enhanced prompt message
+			window.dispatchEvent(
+				new MessageEvent("message", {
+					data: {
+						type: "enhancedPrompt",
+						text: "Enhanced test prompt",
+					},
+				}),
+			)
+
+			// Verify fallback to setInputValue was used
 			expect(setInputValue).toHaveBeenCalledWith("Enhanced test prompt")
 		})
+
+		it("should not crash when textarea ref is not available", () => {
+			const setInputValue = vi.fn()
+
+			render(<ChatTextArea {...defaultProps} setInputValue={setInputValue} />)
+
+			// Simulate receiving enhanced prompt message when textarea ref might not be ready
+			expect(() => {
+				window.dispatchEvent(
+					new MessageEvent("message", {
+						data: {
+							type: "enhancedPrompt",
+							text: "Enhanced test prompt",
+						},
+					}),
+				)
+			}).not.toThrow()
+		})
 	})
 
 	describe("multi-file drag and drop", () => {
diff --git a/webview-ui/vitest.setup.ts b/webview-ui/vitest.setup.ts
index afa37bd96d4..12210f0ec20 100644
--- a/webview-ui/vitest.setup.ts
+++ b/webview-ui/vitest.setup.ts
@@ -1,6 +1,12 @@
 import "@testing-library/jest-dom"
 import "@testing-library/jest-dom/vitest"
 
+// Force React into development mode for tests
+// This is needed to enable act(...) function in React Testing Library
+globalThis.process = globalThis.process || {}
+globalThis.process.env = globalThis.process.env || {}
+globalThis.process.env.NODE_ENV = "development"
+
 class MockResizeObserver {
 	observe() {}
 	unobserve() {}