diff --git a/src/core/mentions/__tests__/resolveImageMentions.spec.ts b/src/core/mentions/__tests__/resolveImageMentions.spec.ts
new file mode 100644
index 00000000000..747c778819f
--- /dev/null
+++ b/src/core/mentions/__tests__/resolveImageMentions.spec.ts
@@ -0,0 +1,193 @@
+import * as path from "path"
+
+import { resolveImageMentions } from "../resolveImageMentions"
+
+vi.mock("../../tools/helpers/imageHelpers", () => ({
+	isSupportedImageFormat: vi.fn((ext: string) =>
+		[".png", ".jpg", ".jpeg", ".gif", ".webp", ".svg", ".bmp", ".ico", ".tiff", ".tif", ".avif"].includes(
+			ext.toLowerCase(),
+		),
+	),
+	readImageAsDataUrlWithBuffer: vi.fn(),
+	validateImageForProcessing: vi.fn(),
+	ImageMemoryTracker: vi.fn().mockImplementation(() => ({
+		getTotalMemoryUsed: vi.fn().mockReturnValue(0),
+		addMemoryUsage: vi.fn(),
+	})),
+	DEFAULT_MAX_IMAGE_FILE_SIZE_MB: 5,
+	DEFAULT_MAX_TOTAL_IMAGE_SIZE_MB: 20,
+}))
+
+import { validateImageForProcessing, readImageAsDataUrlWithBuffer } from "../../tools/helpers/imageHelpers"
+
+const mockReadImageAsDataUrl = vi.mocked(readImageAsDataUrlWithBuffer)
+const mockValidateImage = vi.mocked(validateImageForProcessing)
+
+describe("resolveImageMentions", () => {
+	beforeEach(() => {
+		vi.clearAllMocks()
+		// Default: validation passes
+		mockValidateImage.mockResolvedValue({ isValid: true, sizeInMB: 0.1 })
+	})
+
+	it("should append a data URL when a local png mention is present", async () => {
+		const dataUrl = `data:image/png;base64,${Buffer.from("png-bytes").toString("base64")}`
+		mockReadImageAsDataUrl.mockResolvedValue({ dataUrl, buffer: Buffer.from("png-bytes") })
+
+		const result = await resolveImageMentions({
+			text: "Please look at @/assets/cat.png",
+			images: [],
+			cwd: "/workspace",
+		})
+
+		expect(mockValidateImage).toHaveBeenCalled()
+		expect(mockReadImageAsDataUrl).toHaveBeenCalledWith(path.resolve("/workspace", "assets/cat.png"))
+		expect(result.text).toBe("Please look at @/assets/cat.png")
+		expect(result.images).toEqual([dataUrl])
+	})
+
+	it("should support gif images (matching read_file)", async () => {
+		const dataUrl = `data:image/gif;base64,${Buffer.from("gif-bytes").toString("base64")}`
+		mockReadImageAsDataUrl.mockResolvedValue({ dataUrl, buffer: Buffer.from("gif-bytes") })
+
+		const result = await resolveImageMentions({
+			text: "See @/animation.gif",
+			images: [],
+			cwd: "/workspace",
+		})
+
+		expect(result.images).toEqual([dataUrl])
+	})
+
+	it("should support svg images (matching read_file)", async () => {
+		const dataUrl = `data:image/svg+xml;base64,${Buffer.from("svg-bytes").toString("base64")}`
+		mockReadImageAsDataUrl.mockResolvedValue({ dataUrl, buffer: Buffer.from("svg-bytes") })
+
+		const result = await resolveImageMentions({
+			text: "See @/icon.svg",
+			images: [],
+			cwd: "/workspace",
+		})
+
+		expect(result.images).toEqual([dataUrl])
+	})
+
+	it("should ignore non-image mentions", async () => {
+		const result = await resolveImageMentions({
+			text: "See @/src/index.ts",
+			images: [],
+			cwd: "/workspace",
+		})
+
+		expect(mockReadImageAsDataUrl).not.toHaveBeenCalled()
+		expect(result.images).toEqual([])
+	})
+
+	it("should skip unreadable files (fail-soft)", async () => {
+		mockReadImageAsDataUrl.mockRejectedValue(new Error("ENOENT"))
+
+		const result = await resolveImageMentions({
+			text: "See @/missing.webp",
+			images: [],
+			cwd: "/workspace",
+		})
+
+		expect(result.images).toEqual([])
+	})
+
+	it("should respect rooIgnoreController", async () => {
+		const dataUrl = `data:image/jpeg;base64,${Buffer.from("jpg-bytes").toString("base64")}`
+		mockReadImageAsDataUrl.mockResolvedValue({ dataUrl, buffer: Buffer.from("jpg-bytes") })
+		const rooIgnoreController = {
+			validateAccess: vi.fn().mockReturnValue(false),
+		}
+
+		const result = await resolveImageMentions({
+			text: "See @/secret.jpg",
+			images: [],
+			cwd: "/workspace",
+			rooIgnoreController,
+		})
+
+		expect(rooIgnoreController.validateAccess).toHaveBeenCalledWith("secret.jpg")
+		expect(mockReadImageAsDataUrl).not.toHaveBeenCalled()
+		expect(result.images).toEqual([])
+	})
+
+	it("should dedupe when mention repeats", async () => {
+		const dataUrl = `data:image/png;base64,${Buffer.from("png-bytes").toString("base64")}`
+		mockReadImageAsDataUrl.mockResolvedValue({ dataUrl, buffer: Buffer.from("png-bytes") })
+
+		const result = await resolveImageMentions({
+			text: "@/a.png and again @/a.png",
+			images: [],
+			cwd: "/workspace",
+		})
+
+		expect(result.images).toHaveLength(1)
+	})
+
+	it("should skip images when supportsImages is false", async () => {
+		const dataUrl = `data:image/png;base64,${Buffer.from("png-bytes").toString("base64")}`
+		mockReadImageAsDataUrl.mockResolvedValue({ dataUrl, buffer: Buffer.from("png-bytes") })
+
+		const result = await resolveImageMentions({
+			text: "See @/cat.png",
+			images: [],
+			cwd: "/workspace",
+			supportsImages: false,
+		})
+
+		expect(mockReadImageAsDataUrl).not.toHaveBeenCalled()
+		expect(result.images).toEqual([])
+	})
+
+	it("should skip images that exceed size limits", async () => {
+		mockValidateImage.mockResolvedValue({
+			isValid: false,
+			reason: "size_limit",
+			notice: "Image too large",
+		})
+
+		const result = await resolveImageMentions({
+			text: "See @/huge.png",
+			images: [],
+			cwd: "/workspace",
+		})
+
+		expect(mockValidateImage).toHaveBeenCalled()
+		expect(mockReadImageAsDataUrl).not.toHaveBeenCalled()
+		expect(result.images).toEqual([])
+	})
+
+	it("should skip images that would exceed memory limit", async () => {
+		mockValidateImage.mockResolvedValue({
+			isValid: false,
+			reason: "memory_limit",
+			notice: "Would exceed memory limit",
+		})
+
+		const result = await resolveImageMentions({
+			text: "See @/large.png",
+			images: [],
+			cwd: "/workspace",
+		})
+
+		expect(result.images).toEqual([])
+	})
+
+	it("should pass custom size limits to validation", async () => {
+		const dataUrl = `data:image/png;base64,${Buffer.from("png-bytes").toString("base64")}`
+		mockReadImageAsDataUrl.mockResolvedValue({ dataUrl, buffer: Buffer.from("png-bytes") })
+
+		await resolveImageMentions({
+			text: "See @/cat.png",
+			images: [],
+			cwd: "/workspace",
+			maxImageFileSize: 10,
+			maxTotalImageSize: 50,
+		})
+
+		expect(mockValidateImage).toHaveBeenCalledWith(expect.any(String), true, 10, 50, 0)
+	})
+})
diff --git a/src/core/mentions/index.ts b/src/core/mentions/index.ts
index f038b5b7836..1ee94c2b86c 100644
--- a/src/core/mentions/index.ts
+++ b/src/core/mentions/index.ts
@@ -274,7 +274,13 @@ async function getFileOrFolderContent(
 		const stats = await fs.stat(absPath)
 
 		if (stats.isFile()) {
-			if (rooIgnoreController && !rooIgnoreController.validateAccess(absPath)) {
+			// Avoid trying to include image binary content as text context.
+			// Image mentions are handled separately via image attachment flow.
+			const isBinary = await isBinaryFile(absPath).catch(() => false)
+			if (isBinary) {
+				return `(Binary file ${mentionPath} omitted)`
+			}
+			if (rooIgnoreController && !rooIgnoreController.validateAccess(unescapedPath)) {
 				return `(File ${mentionPath} is ignored by .rooignore)`
 			}
 			try {
diff --git a/src/core/mentions/resolveImageMentions.ts b/src/core/mentions/resolveImageMentions.ts
new file mode 100644
index 00000000000..0a0344348f1
--- /dev/null
+++ b/src/core/mentions/resolveImageMentions.ts
@@ -0,0 +1,145 @@
+import * as path from "path"
+
+import { mentionRegexGlobal, unescapeSpaces } from "../../shared/context-mentions"
+import {
+	isSupportedImageFormat,
+	readImageAsDataUrlWithBuffer,
+	validateImageForProcessing,
+	ImageMemoryTracker,
+	DEFAULT_MAX_IMAGE_FILE_SIZE_MB,
+	DEFAULT_MAX_TOTAL_IMAGE_SIZE_MB,
+} from "../tools/helpers/imageHelpers"
+
+const MAX_IMAGES_PER_MESSAGE = 20
+
+export interface ResolveImageMentionsOptions {
+	text: string
+	images?: string[]
+	cwd: string
+	rooIgnoreController?: { validateAccess: (filePath: string) => boolean }
+	/** Whether the current model supports images. Defaults to true. */
+	supportsImages?: boolean
+	/** Maximum size per image file in MB. Defaults to 5MB. */
+	maxImageFileSize?: number
+	/** Maximum total size of all images in MB. Defaults to 20MB. */
+	maxTotalImageSize?: number
+}
+
+export interface ResolveImageMentionsResult {
+	text: string
+	images: string[]
+}
+
+function isPathWithinCwd(absPath: string, cwd: string): boolean {
+	const rel = path.relative(cwd, absPath)
+	return rel !== "" && !rel.startsWith("..") && !path.isAbsolute(rel)
+}
+
+function dedupePreserveOrder(values: string[]): string[] {
+	const seen = new Set<string>()
+	const result: string[] = []
+	for (const v of values) {
+		if (seen.has(v)) continue
+		seen.add(v)
+		result.push(v)
+	}
+	return result
+}
+
+/**
+ * Resolves local image file mentions like `@/path/to/image.png` found in `text` into `data:image/...;base64,...`
+ * and appends them to the outgoing `images` array.
+ *
+ * Behavior matches the read_file tool:
+ * - Supports the same image formats: png, jpg, jpeg, gif, webp, svg, bmp, ico, tiff, avif
+ * - Respects per-file size limits (default 5MB)
+ * - Respects total memory limits (default 20MB)
+ * - Skips images if model doesn't support them
+ * - Respects `.rooignore` via `rooIgnoreController.validateAccess` when provided
+ */
+export async function resolveImageMentions({
+	text,
+	images,
+	cwd,
+	rooIgnoreController,
+	supportsImages = true,
+	maxImageFileSize = DEFAULT_MAX_IMAGE_FILE_SIZE_MB,
+	maxTotalImageSize = DEFAULT_MAX_TOTAL_IMAGE_SIZE_MB,
+}: ResolveImageMentionsOptions): Promise<ResolveImageMentionsResult> {
+	const existingImages = Array.isArray(images) ? images : []
+	if (existingImages.length >= MAX_IMAGES_PER_MESSAGE) {
+		return { text, images: existingImages.slice(0, MAX_IMAGES_PER_MESSAGE) }
+	}
+
+	// If model doesn't support images, skip image processing entirely
+	if (!supportsImages) {
+		return { text, images: existingImages }
+	}
+
+	const mentions = Array.from(text.matchAll(mentionRegexGlobal))
+		.map((m) => m[1])
+		.filter(Boolean)
+	if (mentions.length === 0) {
+		return { text, images: existingImages }
+	}
+
+	const imageMentions = mentions.filter((mention) => {
+		if (!mention.startsWith("/")) return false
+		const relPath = unescapeSpaces(mention.slice(1))
+		const ext = path.extname(relPath).toLowerCase()
+		return isSupportedImageFormat(ext)
+	})
+
+	if (imageMentions.length === 0) {
+		return { text, images: existingImages }
+	}
+
+	const imageMemoryTracker = new ImageMemoryTracker()
+	const newImages: string[] = []
+
+	for (const mention of imageMentions) {
+		if (existingImages.length + newImages.length >= MAX_IMAGES_PER_MESSAGE) {
+			break
+		}
+
+		const relPath = unescapeSpaces(mention.slice(1))
+		const absPath = path.resolve(cwd, relPath)
+		if (!isPathWithinCwd(absPath, cwd)) {
+			continue
+		}
+
+		if (rooIgnoreController && !rooIgnoreController.validateAccess(relPath)) {
+			continue
+		}
+
+		// Validate image size limits (matches read_file behavior)
+		try {
+			const validationResult = await validateImageForProcessing(
+				absPath,
+				supportsImages,
+				maxImageFileSize,
+				maxTotalImageSize,
+				imageMemoryTracker.getTotalMemoryUsed(),
+			)
+
+			if (!validationResult.isValid) {
+				// Skip this image due to size/memory limits, but continue processing others
+				continue
+			}
+
+			const { dataUrl } = await readImageAsDataUrlWithBuffer(absPath)
+			newImages.push(dataUrl)
+
+			// Track memory usage
+			if (validationResult.sizeInMB) {
+				imageMemoryTracker.addMemoryUsage(validationResult.sizeInMB)
+			}
+		} catch {
+			// Fail-soft: skip unreadable/missing files.
+			continue
+		}
+	}
+
+	const merged = dedupePreserveOrder([...existingImages, ...newImages]).slice(0, MAX_IMAGES_PER_MESSAGE)
+	return { text, images: merged }
+}
diff --git a/src/core/webview/__tests__/ClineProvider.spec.ts b/src/core/webview/__tests__/ClineProvider.spec.ts
index 85e144290f0..f73cf0eb588 100644
--- a/src/core/webview/__tests__/ClineProvider.spec.ts
+++ b/src/core/webview/__tests__/ClineProvider.spec.ts
@@ -3048,7 +3048,7 @@ describe("ClineProvider - Comprehensive Edit/Delete Edge Cases", () => {
 			expect(mockCline.overwriteClineMessages).toHaveBeenCalledWith([mockMessages[0]])
 			expect(mockCline.overwriteApiConversationHistory).toHaveBeenCalledWith([{ ts: 1000 }])
 			// Verify submitUserMessage was called with the edited content
-			expect(mockCline.submitUserMessage).toHaveBeenCalledWith("Edited message with preserved images", undefined)
+			expect(mockCline.submitUserMessage).toHaveBeenCalledWith("Edited message with preserved images", [])
 		})
 
 		test("handles editing messages with file attachments", async () => {
@@ -3101,7 +3101,7 @@ describe("ClineProvider - Comprehensive Edit/Delete Edge Cases", () => {
 			})
 
 			expect(mockCline.overwriteClineMessages).toHaveBeenCalled()
-			expect(mockCline.submitUserMessage).toHaveBeenCalledWith("Edited message with file attachment", undefined)
+			expect(mockCline.submitUserMessage).toHaveBeenCalledWith("Edited message with file attachment", [])
 		})
 	})
 
@@ -3632,7 +3632,7 @@ describe("ClineProvider - Comprehensive Edit/Delete Edge Cases", () => {
 				await messageHandler({ type: "editMessageConfirm", messageTs: 2000, text: largeEditedContent })
 
 				expect(mockCline.overwriteClineMessages).toHaveBeenCalled()
-				expect(mockCline.submitUserMessage).toHaveBeenCalledWith(largeEditedContent, undefined)
+				expect(mockCline.submitUserMessage).toHaveBeenCalledWith(largeEditedContent, [])
 			})
 
 			test("handles deleting messages with large payloads", async () => {
diff --git a/src/core/webview/__tests__/webviewMessageHandler.checkpoint.spec.ts b/src/core/webview/__tests__/webviewMessageHandler.checkpoint.spec.ts
index a0687d6cc19..2b2b0f78b1d 100644
--- a/src/core/webview/__tests__/webviewMessageHandler.checkpoint.spec.ts
+++ b/src/core/webview/__tests__/webviewMessageHandler.checkpoint.spec.ts
@@ -55,6 +55,10 @@ describe("webviewMessageHandler - checkpoint operations", () => {
 			contextProxy: {
 				globalStorageUri: { fsPath: "/test/storage" },
 			},
+			getState: vi.fn().mockResolvedValue({
+				maxImageFileSize: 5,
+				maxTotalImageSize: 20,
+			}),
 		}
 	})
 
@@ -124,7 +128,7 @@ describe("webviewMessageHandler - checkpoint operations", () => {
 				operation: "edit",
 				editData: {
 					editedContent: "Edited checkpoint message",
-					images: undefined,
+					images: [],
 					apiConversationHistoryIndex: 0,
 				},
 			})
diff --git a/src/core/webview/__tests__/webviewMessageHandler.edit.spec.ts b/src/core/webview/__tests__/webviewMessageHandler.edit.spec.ts
index dfbce361e45..d1d7bba1283 100644
--- a/src/core/webview/__tests__/webviewMessageHandler.edit.spec.ts
+++ b/src/core/webview/__tests__/webviewMessageHandler.edit.spec.ts
@@ -70,6 +70,10 @@ describe("webviewMessageHandler - Edit Message with Timestamp Fallback", () => {
 				globalStorageUri: { fsPath: "/mock/storage" },
 			},
 			log: vi.fn(),
+			getState: vi.fn().mockResolvedValue({
+				maxImageFileSize: 5,
+				maxTotalImageSize: 20,
+			}),
 		} as unknown as ClineProvider
 	})
 
diff --git a/src/core/webview/__tests__/webviewMessageHandler.imageMentions.integration.spec.ts b/src/core/webview/__tests__/webviewMessageHandler.imageMentions.integration.spec.ts
new file mode 100644
index 00000000000..277e56626ad
--- /dev/null
+++ b/src/core/webview/__tests__/webviewMessageHandler.imageMentions.integration.spec.ts
@@ -0,0 +1,130 @@
+import * as fs from "fs/promises"
+import * as path from "path"
+import * as os from "os"
+
+// Must mock dependencies before importing the handler module.
+vi.mock("../../../api/providers/fetchers/modelCache")
+
+import { webviewMessageHandler } from "../webviewMessageHandler"
+import type { ClineProvider } from "../ClineProvider"
+
+vi.mock("vscode", () => ({
+	window: {
+		showInformationMessage: vi.fn(),
+		showErrorMessage: vi.fn(),
+	},
+	workspace: {
+		workspaceFolders: [{ uri: { fsPath: "/mock/workspace" } }],
+	},
+}))
+
+// Mock imageHelpers - use actual implementations for functions that need real file access
+vi.mock("../../tools/helpers/imageHelpers", async (importOriginal) => {
+	const actual = await importOriginal<typeof import("../../tools/helpers/imageHelpers")>()
+	return {
+		...actual,
+		validateImageForProcessing: vi.fn().mockResolvedValue({ isValid: true, sizeInMB: 0.001 }),
+		ImageMemoryTracker: vi.fn().mockImplementation(() => ({
+			getTotalMemoryUsed: vi.fn().mockReturnValue(0),
+			addMemoryUsage: vi.fn(),
+		})),
+	}
+})
+
+describe("webviewMessageHandler - image mentions (integration)", () => {
+	it("resolves image mentions for newTask and passes images to createTask", async () => {
+		const tmpRoot = await fs.mkdtemp(path.join(os.tmpdir(), "roo-image-mentions-"))
+		try {
+			const imgBytes = Buffer.from("png-bytes")
+			await fs.writeFile(path.join(tmpRoot, "cat.png"), imgBytes)
+
+			const mockProvider = {
+				cwd: tmpRoot,
+				getCurrentTask: vi.fn().mockReturnValue(undefined),
+				createTask: vi.fn().mockResolvedValue(undefined),
+				postMessageToWebview: vi.fn().mockResolvedValue(undefined),
+				getState: vi.fn().mockResolvedValue({
+					maxImageFileSize: 5,
+					maxTotalImageSize: 20,
+				}),
+			} as unknown as ClineProvider
+
+			await webviewMessageHandler(mockProvider, {
+				type: "newTask",
+				text: "Please look at @/cat.png",
+				images: [],
+			} as any)
+
+			expect(mockProvider.createTask).toHaveBeenCalledWith("Please look at @/cat.png", [
+				`data:image/png;base64,${imgBytes.toString("base64")}`,
+			])
+		} finally {
+			await fs.rm(tmpRoot, { recursive: true, force: true })
+		}
+	})
+
+	it("resolves image mentions for askResponse and passes images to handleWebviewAskResponse", async () => {
+		const tmpRoot = await fs.mkdtemp(path.join(os.tmpdir(), "roo-image-mentions-"))
+		try {
+			const imgBytes = Buffer.from("jpg-bytes")
+			await fs.writeFile(path.join(tmpRoot, "cat.jpg"), imgBytes)
+
+			const handleWebviewAskResponse = vi.fn()
+			const mockProvider = {
+				cwd: tmpRoot,
+				getCurrentTask: vi.fn().mockReturnValue({
+					cwd: tmpRoot,
+					handleWebviewAskResponse,
+				}),
+				getState: vi.fn().mockResolvedValue({
+					maxImageFileSize: 5,
+					maxTotalImageSize: 20,
+				}),
+			} as unknown as ClineProvider
+
+			await webviewMessageHandler(mockProvider, {
+				type: "askResponse",
+				askResponse: "messageResponse",
+				text: "Please look at @/cat.jpg",
+				images: [],
+			} as any)
+
+			expect(handleWebviewAskResponse).toHaveBeenCalledWith("messageResponse", "Please look at @/cat.jpg", [
+				`data:image/jpeg;base64,${imgBytes.toString("base64")}`,
+			])
+		} finally {
+			await fs.rm(tmpRoot, { recursive: true, force: true })
+		}
+	})
+
+	it("resolves gif image mentions (matching read_file behavior)", async () => {
+		const tmpRoot = await fs.mkdtemp(path.join(os.tmpdir(), "roo-image-mentions-"))
+		try {
+			const imgBytes = Buffer.from("gif-bytes")
+			await fs.writeFile(path.join(tmpRoot, "animation.gif"), imgBytes)
+
+			const mockProvider = {
+				cwd: tmpRoot,
+				getCurrentTask: vi.fn().mockReturnValue(undefined),
+				createTask: vi.fn().mockResolvedValue(undefined),
+				postMessageToWebview: vi.fn().mockResolvedValue(undefined),
+				getState: vi.fn().mockResolvedValue({
+					maxImageFileSize: 5,
+					maxTotalImageSize: 20,
+				}),
+			} as unknown as ClineProvider
+
+			await webviewMessageHandler(mockProvider, {
+				type: "newTask",
+				text: "See @/animation.gif",
+				images: [],
+			} as any)
+
+			expect(mockProvider.createTask).toHaveBeenCalledWith("See @/animation.gif", [
+				`data:image/gif;base64,${imgBytes.toString("base64")}`,
+			])
+		} finally {
+			await fs.rm(tmpRoot, { recursive: true, force: true })
+		}
+	})
+})
diff --git a/src/core/webview/__tests__/webviewMessageHandler.spec.ts b/src/core/webview/__tests__/webviewMessageHandler.spec.ts
index f724558ae6a..8e8401eb924 100644
--- a/src/core/webview/__tests__/webviewMessageHandler.spec.ts
+++ b/src/core/webview/__tests__/webviewMessageHandler.spec.ts
@@ -96,6 +96,15 @@ vi.mock("../../../utils/fs")
 vi.mock("../../../utils/path")
 vi.mock("../../../utils/globalContext")
 
+vi.mock("../../mentions/resolveImageMentions", () => ({
+	resolveImageMentions: vi.fn(async ({ text, images }: { text: string; images?: string[] }) => ({
+		text,
+		images: [...(images ?? []), "data:image/png;base64,from-mention"],
+	})),
+}))
+
+import { resolveImageMentions } from "../../mentions/resolveImageMentions"
+
 describe("webviewMessageHandler - requestLmStudioModels", () => {
 	beforeEach(() => {
 		vi.clearAllMocks()
@@ -138,6 +147,37 @@ describe("webviewMessageHandler - requestLmStudioModels", () => {
 	})
 })
 
+describe("webviewMessageHandler - image mentions", () => {
+	beforeEach(() => {
+		vi.clearAllMocks()
+		mockClineProvider.getState = vi.fn().mockResolvedValue({
+			maxImageFileSize: 5,
+			maxTotalImageSize: 20,
+		})
+	})
+
+	it("should resolve image mentions for askResponse payloads", async () => {
+		const mockHandleWebviewAskResponse = vi.fn()
+		vi.mocked(mockClineProvider.getCurrentTask).mockReturnValue({
+			cwd: "/mock/workspace",
+			rooIgnoreController: undefined,
+			handleWebviewAskResponse: mockHandleWebviewAskResponse,
+		} as any)
+
+		await webviewMessageHandler(mockClineProvider, {
+			type: "askResponse",
+			askResponse: "messageResponse",
+			text: "See @/img.png",
+			images: [],
+		})
+
+		expect(vi.mocked(resolveImageMentions)).toHaveBeenCalled()
+		expect(mockHandleWebviewAskResponse).toHaveBeenCalledWith("messageResponse", "See @/img.png", [
+			"data:image/png;base64,from-mention",
+		])
+	})
+})
+
 describe("webviewMessageHandler - requestOllamaModels", () => {
 	beforeEach(() => {
 		vi.clearAllMocks()
diff --git a/src/core/webview/webviewMessageHandler.ts b/src/core/webview/webviewMessageHandler.ts
index c08504c576d..4dca1253e42 100644
--- a/src/core/webview/webviewMessageHandler.ts
+++ b/src/core/webview/webviewMessageHandler.ts
@@ -52,6 +52,7 @@ import { exportSettings, importSettingsWithFeedback } from "../config/importExpo
 import { getOpenAiModels } from "../../api/providers/openai"
 import { getVsCodeLmModels } from "../../api/providers/vscode-lm"
 import { openMention } from "../mentions"
+import { resolveImageMentions } from "../mentions/resolveImageMentions"
 import { getWorkspacePath } from "../../utils/path"
 import { Mode, defaultModeSlug } from "../../shared/modes"
 import { getModels, flushModels } from "../../api/providers/fetchers/modelCache"
@@ -77,6 +78,26 @@ export const webviewMessageHandler = async (
 	const getCurrentCwd = () => {
 		return provider.getCurrentTask()?.cwd || provider.cwd
 	}
+
+	/**
+	 * Resolves image file mentions in incoming messages.
+	 * Matches read_file behavior: respects size limits and model capabilities.
+	 */
+	const resolveIncomingImages = async (payload: { text?: string; images?: string[] }) => {
+		const text = payload.text ?? ""
+		const images = payload.images
+		const currentTask = provider.getCurrentTask()
+		const state = await provider.getState()
+		const resolved = await resolveImageMentions({
+			text,
+			images,
+			cwd: getCurrentCwd(),
+			rooIgnoreController: currentTask?.rooIgnoreController,
+			maxImageFileSize: state.maxImageFileSize,
+			maxTotalImageSize: state.maxTotalImageSize,
+		})
+		return resolved
+	}
 	/**
 	 * Shared utility to find message indices based on timestamp.
 	 * When multiple messages share the same timestamp (e.g., after condense),
@@ -503,7 +524,8 @@ export const webviewMessageHandler = async (
 			// agentically running promises in old instance don't affect our new
 			// task. This essentially creates a fresh slate for the new task.
 			try {
-				await provider.createTask(message.text, message.images)
+				const resolved = await resolveIncomingImages({ text: message.text, images: message.images })
+				await provider.createTask(resolved.text, resolved.images)
 				// Task created successfully - notify the UI to reset
 				await provider.postMessageToWebview({ type: "invoke", invoke: "newChat" })
 			} catch (error) {
@@ -520,7 +542,12 @@ export const webviewMessageHandler = async (
 			break
 
 		case "askResponse":
-			provider.getCurrentTask()?.handleWebviewAskResponse(message.askResponse!, message.text, message.images)
+			{
+				const resolved = await resolveIncomingImages({ text: message.text, images: message.images })
+				provider
+					.getCurrentTask()
+					?.handleWebviewAskResponse(message.askResponse!, resolved.text, resolved.images)
+			}
 			break
 
 		case "updateSettings":
@@ -1842,11 +1869,12 @@ export const webviewMessageHandler = async (
 			break
 		case "editMessageConfirm":
 			if (message.messageTs && message.text) {
+				const resolved = await resolveIncomingImages({ text: message.text, images: message.images })
 				await handleEditMessageConfirm(
 					message.messageTs,
-					message.text,
+					resolved.text,
 					message.restoreCheckpoint,
-					message.images,
+					resolved.images,
 				)
 			}
 			break
@@ -2991,7 +3019,8 @@ export const webviewMessageHandler = async (
 		 */
 
 		case "queueMessage": {
-			provider.getCurrentTask()?.messageQueueService.addMessage(message.text ?? "", message.images)
+			const resolved = await resolveIncomingImages({ text: message.text, images: message.images })
+			provider.getCurrentTask()?.messageQueueService.addMessage(resolved.text, resolved.images)
 			break
 		}
 		case "removeQueuedMessage": {