diff --git a/src/vs/workbench/contrib/chat/browser/chat.contribution.ts b/src/vs/workbench/contrib/chat/browser/chat.contribution.ts
index b97e3e2188b..01c28b42fdf 100644
--- a/src/vs/workbench/contrib/chat/browser/chat.contribution.ts
+++ b/src/vs/workbench/contrib/chat/browser/chat.contribution.ts
@@ -54,7 +54,7 @@ import { ILanguageModelToolsConfirmationService } from '../common/languageModelT
 import { ILanguageModelToolsService } from '../common/languageModelToolsService.js';
 import { ChatPromptFilesExtensionPointHandler } from '../common/promptSyntax/chatPromptFilesContribution.js';
 import { PromptsConfig } from '../common/promptSyntax/config/config.js';
-import { INSTRUCTIONS_DEFAULT_SOURCE_FOLDER, INSTRUCTION_FILE_EXTENSION, LEGACY_MODE_DEFAULT_SOURCE_FOLDER, LEGACY_MODE_FILE_EXTENSION, PROMPT_DEFAULT_SOURCE_FOLDER, PROMPT_FILE_EXTENSION, PROMPT_POSITRON_SOURCE_FOLDER, MODE_POSITRON_SOURCE_FOLDER } from '../common/promptSyntax/config/promptFileLocations.js';
+import { INSTRUCTIONS_DEFAULT_SOURCE_FOLDER, INSTRUCTION_FILE_EXTENSION, LEGACY_MODE_DEFAULT_SOURCE_FOLDER, LEGACY_MODE_FILE_EXTENSION, PROMPT_DEFAULT_SOURCE_FOLDER, PROMPT_FILE_EXTENSION } from '../common/promptSyntax/config/promptFileLocations.js';
 import { PromptLanguageFeaturesProvider } from '../common/promptSyntax/promptFileContributions.js';
 import { AGENT_DOCUMENTATION_URL, INSTRUCTIONS_DOCUMENTATION_URL, PROMPT_DOCUMENTATION_URL } from '../common/promptSyntax/promptTypes.js';
 import { IPromptsService } from '../common/promptSyntax/service/promptsService.js';
@@ -132,7 +132,8 @@ import { ChatViewsWelcomeHandler } from './viewsWelcome/chatViewsWelcomeHandler.
 // --- Start Positron ---
 import { PositronBuiltinToolsContribution } from './tools/tools.js';
 import { ChatRuntimeSessionContextContribution } from './contrib/chatRuntimeSessionContext.js';
-import { INSTRUCTIONS_POSITRON_SOURCE_FOLDER } from '../common/promptSyntax/config/promptFileLocations.js';
+// eslint-disable-next-line no-duplicate-imports
+import { INSTRUCTIONS_POSITRON_SOURCE_FOLDER, PROMPT_POSITRON_SOURCE_FOLDER, LEGACY_MODE_POSITRON_SOURCE_FOLDER } from '../common/promptSyntax/config/promptFileLocations.js';
 // --- End Positron ---
 
 // Register configuration
@@ -627,8 +628,8 @@ configurationRegistry.registerConfiguration({
 				AGENT_DOCUMENTATION_URL,
 			),
 			default: {
-					// --- Start Positron ---
-				[MODE_POSITRON_SOURCE_FOLDER]: true,
+				// --- Start Positron ---
+				[LEGACY_MODE_POSITRON_SOURCE_FOLDER]: true,
 				// --- End Positron ---
 				[LEGACY_MODE_DEFAULT_SOURCE_FOLDER]: true,
 			},
diff --git a/src/vs/workbench/contrib/chat/common/promptSyntax/config/promptFileLocations.ts b/src/vs/workbench/contrib/chat/common/promptSyntax/config/promptFileLocations.ts
index 122d8c1b6cf..6b05b82a026 100644
--- a/src/vs/workbench/contrib/chat/common/promptSyntax/config/promptFileLocations.ts
+++ b/src/vs/workbench/contrib/chat/common/promptSyntax/config/promptFileLocations.ts
@@ -65,7 +65,8 @@ function isInAgentsFolder(fileUri: URI): boolean {
 // Additional search paths for `.vscode/positron` directory
 export const PROMPT_POSITRON_SOURCE_FOLDER = '.vscode/positron/prompts';
 export const INSTRUCTIONS_POSITRON_SOURCE_FOLDER = '.vscode/positron/instructions';
-export const MODE_POSITRON_SOURCE_FOLDER = '.vscode/positron/chatmodes';
+export const LEGACY_MODE_POSITRON_SOURCE_FOLDER = '.vscode/positron/chatmodes';
+export const AGENTS_POSITRON_SOURCE_FOLDER = '.vscode/positron/agents';
 // --- End Positron ---
 
 /**
diff --git a/src/vs/workbench/contrib/chat/common/promptSyntax/utils/promptFilesLocator.ts b/src/vs/workbench/contrib/chat/common/promptSyntax/utils/promptFilesLocator.ts
index 1ebf5c3c598..ee401d81914 100644
--- a/src/vs/workbench/contrib/chat/common/promptSyntax/utils/promptFilesLocator.ts
+++ b/src/vs/workbench/contrib/chat/common/promptSyntax/utils/promptFilesLocator.ts
@@ -24,6 +24,11 @@ import { Emitter, Event } from '../../../../../../base/common/event.js';
 import { Disposable, DisposableStore } from '../../../../../../base/common/lifecycle.js';
 import { ILogService } from '../../../../../../platform/log/common/log.js';
 
+// --- Start Positron ---
+// eslint-disable-next-line no-duplicate-imports
+import { AGENTS_POSITRON_SOURCE_FOLDER } from '../config/promptFileLocations.js';
+// --- End Positron ---
+
 /**
  * Utility class to locate prompt files.
  */
@@ -104,7 +109,12 @@ export class PromptFilesLocator extends Disposable {
 	}
 
 	public getAgentSourceFolder(): readonly URI[] {
+		// --- Start Positron ---
+		/*
 		return this.toAbsoluteLocations([AGENTS_SOURCE_FOLDER]);
+		*/
+		return this.toAbsoluteLocations([AGENTS_SOURCE_FOLDER, AGENTS_POSITRON_SOURCE_FOLDER]);
+		// --- End Positron ---
 	}
 
 	/**
@@ -189,6 +199,9 @@ export class PromptFilesLocator extends Disposable {
 		const configuredLocations = PromptsConfig.promptSourceFolders(this.configService, type);
 		if (type === PromptsType.agent) {
 			configuredLocations.push(AGENTS_SOURCE_FOLDER);
+			// --- Start Positron ---
+			configuredLocations.push(AGENTS_POSITRON_SOURCE_FOLDER);
+			// --- End Positron ---
 		}
 		const absoluteLocations = this.toAbsoluteLocations(configuredLocations);
 		return absoluteLocations.map(firstNonGlobParentAndPattern);