diff --git a/surfsense_desktop/src/ipc/handlers.ts b/surfsense_desktop/src/ipc/handlers.ts
index cc84a46e0..247d171f5 100644
--- a/surfsense_desktop/src/ipc/handlers.ts
+++ b/surfsense_desktop/src/ipc/handlers.ts
@@ -228,7 +228,7 @@ export function registerIpcHandlers(): void {
 
   ipcMain.handle(
     IPC_CHANNELS.AGENT_FILESYSTEM_SET_SETTINGS,
-    (_event, settings: { mode?: 'cloud' | 'desktop_local_folder'; localRootPath?: string | null }) =>
+    (_event, settings: { mode?: 'cloud' | 'desktop_local_folder'; localRootPaths?: string[] | null }) =>
       setAgentFilesystemSettings(settings)
   );
 
diff --git a/surfsense_desktop/src/modules/agent-filesystem.ts b/surfsense_desktop/src/modules/agent-filesystem.ts
index 9dfe79fb0..afad98f24 100644
--- a/surfsense_desktop/src/modules/agent-filesystem.ts
+++ b/surfsense_desktop/src/modules/agent-filesystem.ts
@@ -1,16 +1,17 @@
 import { app, dialog } from "electron";
-import { mkdir, readFile, writeFile } from "node:fs/promises";
+import { access, mkdir, readFile, writeFile } from "node:fs/promises";
 import { dirname, isAbsolute, join, relative, resolve } from "node:path";
 
 export type AgentFilesystemMode = "cloud" | "desktop_local_folder";
 
 export interface AgentFilesystemSettings {
 	mode: AgentFilesystemMode;
-	localRootPath: string | null;
+	localRootPaths: string[];
 	updatedAt: string;
 }
 
 const SETTINGS_FILENAME = "agent-filesystem-settings.json";
+const MAX_LOCAL_ROOTS = 5;
 
 function getSettingsPath(): string {
 	return join(app.getPath("userData"), SETTINGS_FILENAME);
@@ -19,11 +20,28 @@ function getSettingsPath(): string {
 function getDefaultSettings(): AgentFilesystemSettings {
 	return {
 		mode: "cloud",
-		localRootPath: null,
+		localRootPaths: [],
 		updatedAt: new Date().toISOString(),
 	};
 }
 
+function normalizeLocalRootPaths(paths: unknown): string[] {
+	if (!Array.isArray(paths)) {
+		return [];
+	}
+	const uniquePaths = new Set<string>();
+	for (const path of paths) {
+		if (typeof path !== "string") continue;
+		const trimmed = path.trim();
+		if (!trimmed) continue;
+		uniquePaths.add(trimmed);
+		if (uniquePaths.size >= MAX_LOCAL_ROOTS) {
+			break;
+		}
+	}
+	return [...uniquePaths];
+}
+
 export async function getAgentFilesystemSettings(): Promise<AgentFilesystemSettings> {
 	try {
 		const raw = await readFile(getSettingsPath(), "utf8");
@@ -33,7 +51,7 @@ export async function getAgentFilesystemSettings(): Promise<AgentFilesystemSetti
 		}
 		return {
 			mode: parsed.mode,
-			localRootPath: parsed.localRootPath ?? null,
+			localRootPaths: normalizeLocalRootPaths(parsed.localRootPaths),
 			updatedAt: parsed.updatedAt ?? new Date().toISOString(),
 		};
 	} catch {
@@ -42,7 +60,10 @@ export async function getAgentFilesystemSettings(): Promise<AgentFilesystemSetti
 }
 
 export async function setAgentFilesystemSettings(
-	settings: Partial<Pick<AgentFilesystemSettings, "mode" | "localRootPath">>
+	settings: {
+		mode?: AgentFilesystemMode;
+		localRootPaths?: string[] | null;
+	}
 ): Promise<AgentFilesystemSettings> {
 	const current = await getAgentFilesystemSettings();
 	const nextMode =
@@ -51,8 +72,10 @@ export async function setAgentFilesystemSettings(
 			: current.mode;
 	const next: AgentFilesystemSettings = {
 		mode: nextMode,
-		localRootPath:
-			settings.localRootPath === undefined ? current.localRootPath : settings.localRootPath,
+		localRootPaths:
+			settings.localRootPaths === undefined
+				? current.localRootPaths
+				: normalizeLocalRootPaths(settings.localRootPaths ?? []),
 		updatedAt: new Date().toISOString(),
 	};
 
@@ -101,20 +124,45 @@ function toVirtualPath(rootPath: string, absolutePath: string): string {
 
 async function resolveCurrentRootPath(): Promise<string> {
 	const settings = await getAgentFilesystemSettings();
-	if (!settings.localRootPath) {
-		throw new Error("No local filesystem root selected");
+	if (settings.localRootPaths.length === 0) {
+		throw new Error("No local filesystem roots selected");
 	}
-	return settings.localRootPath;
+	return settings.localRootPaths[0];
+}
+
+async function resolveCurrentRootPaths(): Promise<string[]> {
+	const settings = await getAgentFilesystemSettings();
+	if (settings.localRootPaths.length === 0) {
+		throw new Error("No local filesystem roots selected");
+	}
+	return settings.localRootPaths;
 }
 
 export async function readAgentLocalFileText(
 	virtualPath: string
 ): Promise<{ path: string; content: string }> {
-	const rootPath = await resolveCurrentRootPath();
-	const absolutePath = resolveVirtualPath(rootPath, virtualPath);
-	const content = await readFile(absolutePath, "utf8");
+	const rootPaths = await resolveCurrentRootPaths();
+	for (const rootPath of rootPaths) {
+		const absolutePath = resolveVirtualPath(rootPath, virtualPath);
+		try {
+			const content = await readFile(absolutePath, "utf8");
+			return {
+				path: toVirtualPath(rootPath, absolutePath),
+				content,
+			};
+		} catch (error) {
+			if ((error as NodeJS.ErrnoException).code === "ENOENT") {
+				continue;
+			}
+			throw error;
+		}
+	}
+	// Keep the same relative virtual path in the error context.
+	const fallbackRootPath = await resolveCurrentRootPath();
+	const fallbackAbsolutePath = resolveVirtualPath(fallbackRootPath, virtualPath);
+	const content = await readFile(fallbackAbsolutePath, "utf8");
 	return {
-		path: toVirtualPath(rootPath, absolutePath),
+		path: toVirtualPath(fallbackRootPath, fallbackAbsolutePath),
 		content,
 	};
 }
@@ -123,11 +171,25 @@ export async function writeAgentLocalFileText(
 	virtualPath: string,
 	content: string
 ): Promise<{ path: string }> {
-	const rootPath = await resolveCurrentRootPath();
-	const absolutePath = resolveVirtualPath(rootPath, virtualPath);
-	await mkdir(dirname(absolutePath), { recursive: true });
-	await writeFile(absolutePath, content, "utf8");
+	const rootPaths = await resolveCurrentRootPaths();
+	let selectedRootPath = rootPaths[0];
+	let selectedAbsolutePath = resolveVirtualPath(selectedRootPath, virtualPath);
+
+	for (const rootPath of rootPaths) {
+		const absolutePath = resolveVirtualPath(rootPath, virtualPath);
+		try {
+			await access(absolutePath);
+			selectedRootPath = rootPath;
+			selectedAbsolutePath = absolutePath;
+			break;
+		} catch {
+			// Keep searching for an existing file path across selected roots.
+		}
+	}
+
+	await mkdir(dirname(selectedAbsolutePath), { recursive: true });
+	await writeFile(selectedAbsolutePath, content, "utf8");
 	return {
-		path: toVirtualPath(rootPath, absolutePath),
+		path: toVirtualPath(selectedRootPath, selectedAbsolutePath),
 	};
 }
diff --git a/surfsense_desktop/src/preload.ts b/surfsense_desktop/src/preload.ts
index 9fc213bfa..f7aaf9633 100644
--- a/surfsense_desktop/src/preload.ts
+++ b/surfsense_desktop/src/preload.ts
@@ -110,7 +110,7 @@ contextBridge.exposeInMainWorld('electronAPI', {
     ipcRenderer.invoke(IPC_CHANNELS.AGENT_FILESYSTEM_GET_SETTINGS),
   setAgentFilesystemSettings: (settings: {
     mode?: "cloud" | "desktop_local_folder";
-    localRootPath?: string | null;
+    localRootPaths?: string[] | null;
   }) => ipcRenderer.invoke(IPC_CHANNELS.AGENT_FILESYSTEM_SET_SETTINGS, settings),
   pickAgentFilesystemRoot: () => ipcRenderer.invoke(IPC_CHANNELS.AGENT_FILESYSTEM_PICK_ROOT),
 });
diff --git a/surfsense_web/app/dashboard/[search_space_id]/new-chat/[[...chat_id]]/page.tsx b/surfsense_web/app/dashboard/[search_space_id]/new-chat/[[...chat_id]]/page.tsx
index bdb77ade2..616637a49 100644
--- a/surfsense_web/app/dashboard/[search_space_id]/new-chat/[[...chat_id]]/page.tsx
+++ b/surfsense_web/app/dashboard/[search_space_id]/new-chat/[[...chat_id]]/page.tsx
@@ -660,7 +660,7 @@ export default function NewChatPage() {
 				const selection = await getAgentFilesystemSelection();
 				if (
 					selection.filesystem_mode === "desktop_local_folder" &&
-					!selection.local_filesystem_root
+					(!selection.local_filesystem_roots || selection.local_filesystem_roots.length === 0)
 				) {
 					toast.error("Select a local folder before using Local Folder mode.");
 					return;
@@ -702,7 +702,7 @@ export default function NewChatPage() {
 						search_space_id: searchSpaceId,
 						filesystem_mode: selection.filesystem_mode,
 						client_platform: selection.client_platform,
-						local_filesystem_root: selection.local_filesystem_root,
+						local_filesystem_roots: selection.local_filesystem_roots,
 						messages: messageHistory,
 						mentioned_document_ids: hasDocumentIds ? mentionedDocumentIds.document_ids : undefined,
 						mentioned_surfsense_doc_ids: hasSurfsenseDocIds
@@ -1098,7 +1098,7 @@ export default function NewChatPage() {
 						decisions,
 						filesystem_mode: selection.filesystem_mode,
 						client_platform: selection.client_platform,
-						local_filesystem_root: selection.local_filesystem_root,
+						local_filesystem_roots: selection.local_filesystem_roots,
 					}),
 					signal: controller.signal,
 				});
@@ -1435,7 +1435,7 @@ export default function NewChatPage() {
 						disabled_tools: disabledTools.length > 0 ? disabledTools : undefined,
 						filesystem_mode: selection.filesystem_mode,
 						client_platform: selection.client_platform,
-						local_filesystem_root: selection.local_filesystem_root,
+						local_filesystem_roots: selection.local_filesystem_roots,
 					}),
 					signal: controller.signal,
 				});
diff --git a/surfsense_web/lib/agent-filesystem.ts b/surfsense_web/lib/agent-filesystem.ts
index 6bfb5d131..c9096a294 100644
--- a/surfsense_web/lib/agent-filesystem.ts
+++ b/surfsense_web/lib/agent-filesystem.ts
@@ -4,7 +4,7 @@ export type ClientPlatform = "web" | "desktop";
 export interface AgentFilesystemSelection {
 	filesystem_mode: AgentFilesystemMode;
 	client_platform: ClientPlatform;
-	local_filesystem_root?: string;
+	local_filesystem_roots?: string[];
 }
 
 const DEFAULT_SELECTION: AgentFilesystemSelection = {
@@ -24,11 +24,12 @@ export async function getAgentFilesystemSelection(): Promise<AgentFilesystemSele
 	}
 	try {
 		const settings = await window.electronAPI.getAgentFilesystemSettings();
-		if (settings.mode === "desktop_local_folder" && settings.localRootPath) {
+		const firstLocalRootPath = settings.localRootPaths[0];
+		if (settings.mode === "desktop_local_folder" && firstLocalRootPath) {
 			return {
 				filesystem_mode: "desktop_local_folder",
 				client_platform: "desktop",
-				local_filesystem_root: settings.localRootPath,
+				local_filesystem_roots: settings.localRootPaths,
 			};
 		}
 		return {
diff --git a/surfsense_web/types/window.d.ts b/surfsense_web/types/window.d.ts
index fe80ef8c0..fb9db1906 100644
--- a/surfsense_web/types/window.d.ts
+++ b/surfsense_web/types/window.d.ts
@@ -45,7 +45,7 @@ type AgentFilesystemMode = "cloud" | "desktop_local_folder";
 
 interface AgentFilesystemSettings {
 	mode: AgentFilesystemMode;
-	localRootPath: string | null;
+	localRootPaths: string[];
 	updatedAt: string;
 }
 
@@ -149,7 +149,7 @@ interface ElectronAPI {
 	getAgentFilesystemSettings: () => Promise<AgentFilesystemSettings>;
 	setAgentFilesystemSettings: (settings: {
 		mode?: AgentFilesystemMode;
-		localRootPath?: string | null;
+		localRootPaths?: string[] | null;
 	}) => Promise<AgentFilesystemSettings>;
 	pickAgentFilesystemRoot: () => Promise<string | null>;
 }