diff --git a/packages/cli/src/cmd/dev/index.ts b/packages/cli/src/cmd/dev/index.ts
index dca47eb20..5d2132b28 100644
--- a/packages/cli/src/cmd/dev/index.ts
+++ b/packages/cli/src/cmd/dev/index.ts
@@ -58,16 +58,39 @@ function normalizeOrgId(orgId: string | undefined): string | undefined {
 	return trimmed ? trimmed : undefined;
 }
 
+const DEV_ORG_ENV_ALIASES = [
+	'AGENTUITY_ORGID',
+	'AGENTUITY_ORG_ID',
+	'AGENTUITY_CLOUD_ORG_ID',
+] as const;
+
+function envOrgId(env: Readonly<Record<string, string | undefined>>): string | undefined {
+	for (const name of DEV_ORG_ENV_ALIASES) {
+		const value = normalizeOrgId(env[name]);
+		if (value) return value;
+	}
+	return undefined;
+}
+
 export function resolveDevOrgId(options: ResolveDevOrgIdOptions): string | undefined {
 	return (
 		normalizeOrgId(options.projectConfig?.orgId) ??
-		normalizeOrgId(options.env.AGENTUITY_ORGID) ??
-		normalizeOrgId(options.env.AGENTUITY_ORG_ID) ??
-		normalizeOrgId(options.env.AGENTUITY_CLOUD_ORG_ID) ??
+		envOrgId(options.env) ??
 		normalizeOrgId(options.config?.preferences?.orgId)
 	);
 }
 
+/** Materialize the resolved org under every known alias so readers agree. */
+export function applyDevOrgEnv(
+	env: Record<string, string | undefined>,
+	orgId: string | undefined
+): void {
+	if (!orgId) return;
+	for (const name of DEV_ORG_ENV_ALIASES) {
+		env[name] = orgId;
+	}
+}
+
 export const command = createCommand({
 	name: 'dev',
 	description: 'Run the project development server',
@@ -172,17 +195,11 @@ export const command = createCommand({
 			env.AGENTUITY_CATALYST_URL = config.overrides.catalyst_url;
 		}
 
-		// Load agentuity.json (if present) so we can surface the project's
-		// orgId to the dev process. The aigateway client and other service
-		// clients accept orgId as a constructor option but otherwise have no
-		// way to pick it up under `agentuity dev`. Other parts of the platform
-		// (pi, coder-tui) already read AGENTUITY_ORGID from env, so we match
-		// that name here.
+		// Materialize the resolved org under every known alias so downstream
+		// readers agree regardless of which name they check.
 		const projectConfig = await tryLoadProjectConfig(rootDir, config);
 		const orgId = resolveDevOrgId({ env, projectConfig, config });
-		if (orgId && !normalizeOrgId(env.AGENTUITY_ORGID)) {
-			env.AGENTUITY_ORGID = orgId;
-		}
+		applyDevOrgEnv(env, orgId);
 
 		// Inject AI Gateway env vars so LLM SDKs route through Agentuity
 		const gatewayInjected = injectGatewayEnv(env, logger);
diff --git a/packages/cli/test/cmd/dev/org-id.test.ts b/packages/cli/test/cmd/dev/org-id.test.ts
index 5119ee97f..0400e55cb 100644
--- a/packages/cli/test/cmd/dev/org-id.test.ts
+++ b/packages/cli/test/cmd/dev/org-id.test.ts
@@ -1,5 +1,5 @@
 import { describe, expect, test } from 'bun:test';
-import { resolveDevOrgId } from '../../../src/cmd/dev/index.ts';
+import { applyDevOrgEnv, resolveDevOrgId } from '../../../src/cmd/dev/index.ts';
 
 describe('resolveDevOrgId', () => {
 	test('prefers project org ID over env and config values', () => {
@@ -49,3 +49,77 @@ describe('resolveDevOrgId', () => {
 		).toBe('org_alt');
 	});
 });
+
+describe('applyDevOrgEnv', () => {
+	test('publishes the resolved org under every org env alias', () => {
+		const env: Record<string, string | undefined> = {};
+		applyDevOrgEnv(env, 'org_project');
+		expect(env.AGENTUITY_ORGID).toBe('org_project');
+		expect(env.AGENTUITY_ORG_ID).toBe('org_project');
+		expect(env.AGENTUITY_CLOUD_ORG_ID).toBe('org_project');
+	});
+
+	test('overwrites stale shell aliases with the resolved org', () => {
+		const env: Record<string, string | undefined> = {
+			AGENTUITY_ORG_ID: 'org_stale',
+			AGENTUITY_CLOUD_ORG_ID: 'org_other',
+		};
+		applyDevOrgEnv(env, 'org_project');
+		expect(env.AGENTUITY_ORGID).toBe('org_project');
+		expect(env.AGENTUITY_ORG_ID).toBe('org_project');
+		expect(env.AGENTUITY_CLOUD_ORG_ID).toBe('org_project');
+	});
+
+	test('overwrites blank aliases', () => {
+		const env: Record<string, string | undefined> = {
+			AGENTUITY_ORGID: '',
+			AGENTUITY_CLOUD_ORG_ID: '  ',
+		};
+		applyDevOrgEnv(env, 'org_project');
+		expect(env.AGENTUITY_ORGID).toBe('org_project');
+		expect(env.AGENTUITY_ORG_ID).toBe('org_project');
+		expect(env.AGENTUITY_CLOUD_ORG_ID).toBe('org_project');
+	});
+
+	test('does nothing without a resolved org', () => {
+		const env: Record<string, string | undefined> = {
+			AGENTUITY_ORG_ID: 'org_shell',
+		};
+		applyDevOrgEnv(env, undefined);
+		expect(env).toEqual({ AGENTUITY_ORG_ID: 'org_shell' });
+	});
+});
+
+describe('resolveDevOrgId + applyDevOrgEnv', () => {
+	test('project org wins and is written to every alias over stale shell env', () => {
+		const env: Record<string, string | undefined> = {
+			AGENTUITY_ORG_ID: 'org_stale',
+		};
+		const orgId = resolveDevOrgId({
+			env,
+			projectConfig: { orgId: 'org_project' },
+			config: null,
+		});
+		applyDevOrgEnv(env, orgId);
+		expect(orgId).toBe('org_project');
+		expect(env.AGENTUITY_ORGID).toBe('org_project');
+		expect(env.AGENTUITY_ORG_ID).toBe('org_project');
+		expect(env.AGENTUITY_CLOUD_ORG_ID).toBe('org_project');
+	});
+
+	test('env-only resolution rewrites every alias to the resolved value', () => {
+		const env: Record<string, string | undefined> = {
+			AGENTUITY_ORG_ID: 'org_shell',
+		};
+		const orgId = resolveDevOrgId({
+			env,
+			projectConfig: null,
+			config: null,
+		});
+		applyDevOrgEnv(env, orgId);
+		expect(orgId).toBe('org_shell');
+		expect(env.AGENTUITY_ORGID).toBe('org_shell');
+		expect(env.AGENTUITY_ORG_ID).toBe('org_shell');
+		expect(env.AGENTUITY_CLOUD_ORG_ID).toBe('org_shell');
+	});
+});