diff --git a/api/src/app.ts b/api/src/app.ts
index 25a1ef1653..e851e17ae2 100644
--- a/api/src/app.ts
+++ b/api/src/app.ts
@@ -7,7 +7,6 @@ import { createRequire } from 'node:module';
 import path from 'path';
 import qs from 'qs';
 import { registerAuthProviders } from './auth.js';
-import { flushCaches } from './cache.js';
 import activityRouter from './controllers/activity.js';
 import assetsRouter from './controllers/assets.js';
 import authRouter from './controllers/auth.js';
@@ -91,8 +90,6 @@ export default async function createApp(): Promise<express.Application> {
 		logger.warn(`Database migrations have not all been run`);
 	}
 
-	await flushCaches();
-
 	await registerAuthProviders();
 
 	const extensionManager = getExtensionManager();
diff --git a/api/src/database/migrations/run.ts b/api/src/database/migrations/run.ts
index 1d5d5d79aa..2ab03a5917 100644
--- a/api/src/database/migrations/run.ts
+++ b/api/src/database/migrations/run.ts
@@ -5,6 +5,7 @@ import { orderBy } from 'lodash-es';
 import { dirname } from 'node:path';
 import { fileURLToPath } from 'node:url';
 import path from 'path';
+import { flushCaches } from '../../cache.js';
 import env from '../../env.js';
 import logger from '../../logger.js';
 import type { Migration } from '../../types/index.js';
@@ -77,6 +78,8 @@ export default async function run(database: Knex, direction: 'up' | 'down' | 'la
 
 		await up(database);
 		await database.insert({ version: nextVersion.version, name: nextVersion.name }).into('directus_migrations');
+
+		await flushCaches(true);
 	}
 
 	async function down() {
@@ -100,11 +103,16 @@ export default async function run(database: Knex, direction: 'up' | 'down' | 'la
 
 		await down(database);
 		await database('directus_migrations').delete().where({ version: migration.version });
+
+		await flushCaches(true);
 	}
 
 	async function latest() {
+		let needsCacheFlush = false;
+
 		for (const migration of migrations) {
 			if (migration.completed === false) {
+				needsCacheFlush = true;
 				const { up } = await import(`file://${migration.file}`);
 
 				if (log) {
@@ -115,5 +123,9 @@ export default async function run(database: Knex, direction: 'up' | 'down' | 'la
 				await database.insert({ version: migration.version, name: migration.name }).into('directus_migrations');
 			}
 		}
+
+		if (needsCacheFlush) {
+			await flushCaches(true);
+		}
 	}
 }
diff --git a/api/src/utils/get-cache-key.test.ts b/api/src/utils/get-cache-key.test.ts
index 963878d74b..fe93c55e4a 100644
--- a/api/src/utils/get-cache-key.test.ts
+++ b/api/src/utils/get-cache-key.test.ts
@@ -3,6 +3,8 @@ import { afterEach, beforeAll, describe, expect, SpyInstance, test, vi } from 'v
 import { getCacheKey } from './get-cache-key.js';
 import * as getGraphqlQueryUtil from './get-graphql-query-and-variables.js';
 
+vi.mock('./package.js', () => ({ version: '1.2.3' }));
+
 const baseUrl = 'http://localhost';
 const restUrl = `${baseUrl}/items/example`;
 const graphQlUrl = `${baseUrl}/graphql`;
@@ -13,42 +15,42 @@ const requests = [
 	{
 		name: 'as unauthenticated request',
 		params: { method, originalUrl: restUrl },
-		key: '17da8272c9a0ec6eea38a37d6d78bddeb7c79045',
+		key: '20ada3d7cc37fb7e742d2a723f6f1d7a64686d2e',
 	},
 	{
 		name: 'as authenticated request',
 		params: { method, originalUrl: restUrl, accountability },
-		key: '99a6394222a3d7d149ac1662fc2fff506932db58',
+		key: '79daba5bf38b6b80cb4bf4e2de95d6a8380f7927',
 	},
 	{
 		name: 'a request with a fields query',
 		params: { method, originalUrl: restUrl, sanitizedQuery: { fields: ['id', 'name'] } },
-		key: 'aa6e2d8a78de4dfb4af6eaa230d1cd9b7d31ed19',
+		key: 'e1839f7379b39188622e797fdbe2e3e6d477cbdc',
 	},
 	{
 		name: 'a request with a filter query',
 		params: { method, originalUrl: restUrl, sanitizedQuery: { filter: { name: { _eq: 'test' } } } },
-		key: 'd7eb8970f0429e1cf85e12eb5bb8669f618b09d3',
+		key: '0bcc9af5f628db85043133e59226b2de154d7183',
 	},
 	{
 		name: 'a GraphQL GET query request',
 		params: { method, originalUrl: graphQlUrl, query: { query: 'query { test { id } }' } },
-		key: '201731b75c627c60554512d819b6935b54c73814',
+		key: '14bc276cf21e2d22334b84841533e2c8e1bba9bd',
 	},
 	{
 		name: 'a GraphQL POST query request',
 		params: { method: 'POST', originalUrl: graphQlUrl, body: { query: 'query { test { name } }' } },
-		key: '64eb0c48ea69d0863ff930398f29b5c7884f88f7',
+		key: 'c5bf03e138e0f7bbaa50dde9cad554bef47a81d2',
 	},
 	{
 		name: 'an authenticated GraphQL GET query request',
 		params: { method, originalUrl: graphQlUrl, accountability, query: { query: 'query { test { id } }' } },
-		key: '9bc52c98dcf2de04c64589f52e0ada1e38d53a90',
+		key: '981f27be4c0cfed0b4eca6ac2514f6629aea6be1',
 	},
 	{
 		name: 'an authenticated GraphQL POST query request',
 		params: { method: 'POST', originalUrl: graphQlUrl, accountability, body: { query: 'query { test { name } }' } },
-		key: '051ea77ce5ba71bbc88bcb567b9ddc602b585c13',
+		key: '358336a2c61f7ea2b41b5c1566bbebe692be601d',
 	},
 ];
 
diff --git a/api/src/utils/get-cache-key.ts b/api/src/utils/get-cache-key.ts
index 9572b27920..eac3c8680b 100644
--- a/api/src/utils/get-cache-key.ts
+++ b/api/src/utils/get-cache-key.ts
@@ -2,12 +2,14 @@ import type { Request } from 'express';
 import hash from 'object-hash';
 import url from 'url';
 import { getGraphqlQueryAndVariables } from './get-graphql-query-and-variables.js';
+import { version } from './package.js';
 
 export function getCacheKey(req: Request): string {
 	const path = url.parse(req.originalUrl).pathname;
 	const isGraphQl = path?.startsWith('/graphql');
 
 	const info = {
+		version,
 		user: req.accountability?.user || null,
 		path,
 		query: isGraphQl ? getGraphqlQueryAndVariables(req) : req.sanitizedQuery,