diff --git a/src/lib/functions/netlify-function.mjs b/src/lib/functions/netlify-function.mjs
index db77ddd8eb9..ad4bf94fb32 100644
--- a/src/lib/functions/netlify-function.mjs
+++ b/src/lib/functions/netlify-function.mjs
@@ -123,6 +123,12 @@ export default class NetlifyFunction {
     }
   }
 
+  async getBuildData() {
+    await this.buildQueue
+
+    return this.buildData
+  }
+
   // Compares a new set of source files against a previous one, returning an
   // object with two Sets, one with added and the other with deleted files.
   getSrcFilesDiff(newSrcFiles) {
diff --git a/src/lib/functions/registry.mjs b/src/lib/functions/registry.mjs
index d15c8a9420a..efc7cbe4f52 100644
--- a/src/lib/functions/registry.mjs
+++ b/src/lib/functions/registry.mjs
@@ -14,6 +14,7 @@ import { getPathInProject } from '../settings.mjs'
 import NetlifyFunction from './netlify-function.mjs'
 import runtimes from './runtimes/index.mjs'
 
+const DEFAULT_URL_EXPRESSION = /^\/.netlify\/(functions|builders)\/([^/]+).*/
 const ZIP_EXTENSION = '.zip'
 
 export class FunctionsRegistry {
@@ -123,6 +124,32 @@ export class FunctionsRegistry {
   }
 
   async getFunctionForURLPath(urlPath, method) {
+    const defaultURLMatch = urlPath.match(DEFAULT_URL_EXPRESSION)
+
+    if (defaultURLMatch) {
+      const func = this.get(defaultURLMatch[2])
+
+      if (!func) {
+        return
+      }
+
+      const { routes = [] } = await func.getBuildData()
+
+      if (routes.length !== 0) {
+        const paths = routes.map((route) => chalk.underline(route.pattern)).join(', ')
+
+        warn(
+          `Function ${chalk.yellow(func.name)} cannot be invoked on ${chalk.underline(
+            urlPath,
+          )}, because the function has the following URL paths defined: ${paths}`,
+        )
+
+        return
+      }
+
+      return { func, route: null }
+    }
+
     for (const func of this.functions.values()) {
       const route = await func.matchURLPath(urlPath, method)
 
diff --git a/src/utils/proxy.mjs b/src/utils/proxy.mjs
index 71ce81b2816..25130f450fb 100644
--- a/src/utils/proxy.mjs
+++ b/src/utils/proxy.mjs
@@ -597,18 +597,17 @@ const onRequest = async (
     return proxy.web(req, res, { target: edgeFunctionsProxyURL })
   }
 
-  // Does the request match a function on the fixed URL path?
-  if (isFunction(settings.functionsPort, req.url)) {
-    return proxy.web(req, res, { target: functionsServer })
-  }
-
-  // Does the request match a function on a custom URL path?
-  const functionMatch = functionsRegistry ? await functionsRegistry.getFunctionForURLPath(req.url, req.method) : null
+  const functionMatch = await functionsRegistry.getFunctionForURLPath(req.url, req.method)
 
   if (functionMatch) {
     // Setting an internal header with the function name so that we don't
     // have to match the URL again in the functions server.
-    const headers = { [NFFunctionName]: functionMatch.func.name, [NFFunctionRoute]: functionMatch.route.pattern }
+    /** @type {Record<string, string>} */
+    const headers = { [NFFunctionName]: functionMatch.func.name }
+
+    if (functionMatch.route) {
+      headers[NFFunctionRoute] = functionMatch.route.pattern
+    }
 
     return proxy.web(req, res, { headers, target: functionsServer })
   }
diff --git a/tests/integration/commands/dev/v2-api.test.ts b/tests/integration/commands/dev/v2-api.test.ts
index 2247ae38379..8854a8d5e6d 100644
--- a/tests/integration/commands/dev/v2-api.test.ts
+++ b/tests/integration/commands/dev/v2-api.test.ts
@@ -126,6 +126,14 @@ describe.runIf(gte(version, '18.13.0'))('v2 api', () => {
       expect(await response.text()).toBe(`With expression path: {"sku":"netlify"}`)
     })
 
+    test<FixtureTestContext>('returns 404 when using the default function URL to access a function with custom routes', async ({
+      devServer,
+    }) => {
+      const url = `http://localhost:${devServer.port}/.netlify/functions/custom-path-literal`
+      const response = await fetch(url)
+      expect(response.status).toBe(404)
+    })
+
     describe('handles rewrites to a function', () => {
       test<FixtureTestContext>('rewrite to legacy URL format with `force: true`', async ({ devServer }) => {
         const url = `http://localhost:${devServer.port}/v2-to-legacy-with-force`