diff --git a/src/rollup/plugins/handlers.ts b/src/rollup/plugins/handlers.ts
index e3c6ad20ee..b66931b411 100644
--- a/src/rollup/plugins/handlers.ts
+++ b/src/rollup/plugins/handlers.ts
@@ -1,16 +1,15 @@
 import { hash } from "ohash";
-import type { Nitro } from "../../types";
+import type { Nitro, NitroRouteRules, NitroEventHandler } from "../../types";
 import { virtual } from "./virtual";
 
-const unique = (arr: any[]) => [...new Set(arr)];
-const getImportId = (p: string, lazy?: boolean) =>
-  (lazy ? "_lazy_" : "_") + hash(p).slice(0, 6);
-
 export function handlers(nitro: Nitro) {
   return virtual(
     {
       "#internal/nitro/virtual/server-handlers": () => {
-        const handlers = [...nitro.scannedHandlers, ...nitro.options.handlers];
+        const handlers: NitroEventHandler[] = [
+          ...nitro.scannedHandlers,
+          ...nitro.options.handlers,
+        ];
         if (nitro.options.serveStatic) {
           handlers.unshift({
             middleware: true,
@@ -25,6 +24,9 @@ export function handlers(nitro: Nitro) {
           });
         }
 
+        // If this handler would render a cached route rule then we can also inject a cached event handler
+        extendMiddlewareWithRuleOverlaps(handlers, nitro.options.routeRules);
+
         // Imports take priority
         const imports = unique(
           handlers.filter((h) => !h.lazy).map((h) => h.handler)
@@ -68,3 +70,58 @@ ${handlers
     nitro.vfs
   );
 }
+
+function unique(arr: any[]) {
+  return [...new Set(arr)];
+}
+
+function getImportId(p: string, lazy?: boolean) {
+  return (lazy ? "_lazy_" : "_") + hash(p).slice(0, 6);
+}
+
+const WILDCARD_PATH_RE = /\/\*\*.*$/;
+
+function extendMiddlewareWithRuleOverlaps(
+  handlers: NitroEventHandler[],
+  routeRules: Record<string, NitroRouteRules>
+) {
+  const rules = Object.entries(routeRules);
+  for (const [path, rule] of rules) {
+    // We can ignore this rule if it is not cached and it isn't nested in a cached route
+    if (!rule.cache) {
+      // If we are nested 'within' a cached route, we want to inject a non-cached event handler
+      const isNested = rules.some(
+        ([p, r]) =>
+          r.cache &&
+          WILDCARD_PATH_RE.test(p) &&
+          path.startsWith(p.replace(WILDCARD_PATH_RE, ""))
+      );
+      if (!isNested) {
+        continue;
+      }
+    }
+    for (const [index, handler] of handlers.entries()) {
+      // Skip middleware
+      if (!handler.route || handler.middleware) {
+        continue;
+      }
+      // We will correctly register this rule as a cached route anyway
+      if (handler.route === path) {
+        break;
+      }
+      // We are looking for handlers that will render a route _despite_ not
+      // having an identical path to it
+      if (!WILDCARD_PATH_RE.test(handler.route)) {
+        continue;
+      }
+      if (!path.startsWith(handler.route.replace(WILDCARD_PATH_RE, ""))) {
+        continue;
+      }
+      handlers.splice(index, 0, {
+        ...handler,
+        route: path,
+      });
+      break;
+    }
+  }
+}
diff --git a/test/fixture/routes/rules/[...slug].ts b/test/fixture/routes/rules/[...slug].ts
new file mode 100644
index 0000000000..1e8eacb84f
--- /dev/null
+++ b/test/fixture/routes/rules/[...slug].ts
@@ -0,0 +1 @@
+export default defineEventHandler((event) => event.path);
diff --git a/test/presets/netlify.test.ts b/test/presets/netlify.test.ts
index f24f881dc2..0a79e2988b 100644
--- a/test/presets/netlify.test.ts
+++ b/test/presets/netlify.test.ts
@@ -44,6 +44,10 @@ describe("nitro:preset:netlify", async () => {
       /rules/redirect/obj	https://nitro.unjs.io/	301
       /rules/nested/*	/base	302
       /rules/redirect	/base	302
+      /rules/_/cached/noncached	/.netlify/functions/server 200
+      /rules/_/noncached/cached	/.netlify/builders/server 200
+      /rules/_/cached/*	/.netlify/builders/server 200
+      /rules/_/noncached/*	/.netlify/functions/server 200
       /rules/swr-ttl/*	/.netlify/builders/server 200
       /rules/swr/*	/.netlify/builders/server 200
       /rules/static	/.netlify/builders/server 200
diff --git a/test/presets/node.test.ts b/test/presets/node.test.ts
index 47fe4cc1d2..0496f0ebd6 100644
--- a/test/presets/node.test.ts
+++ b/test/presets/node.test.ts
@@ -1,5 +1,5 @@
 import { resolve } from "pathe";
-import { describe } from "vitest";
+import { describe, it, expect } from "vitest";
 import { startServer, setupTest, testNitro } from "../tests";
 
 describe("nitro:preset:node", async () => {
@@ -12,4 +12,17 @@ describe("nitro:preset:node", async () => {
       return res;
     };
   });
+  it("should handle nested cached route rules", async () => {
+    const cached = await ctx.fetch("/rules/_/noncached/cached");
+    expect(cached.headers.get("etag")).toBeDefined();
+
+    const noncached = await ctx.fetch("/rules/_/noncached/noncached");
+    expect(noncached.headers.get("etag")).toBeNull();
+
+    const cached2 = await ctx.fetch("/rules/_/cached/cached");
+    expect(cached2.headers.get("etag")).toBeDefined();
+
+    const noncached2 = await ctx.fetch("/rules/_/cached/noncached");
+    expect(noncached2.headers.get("etag")).toBeNull();
+  });
 });
diff --git a/test/presets/vercel.test.ts b/test/presets/vercel.test.ts
index 274dfe432a..b47654538d 100644
--- a/test/presets/vercel.test.ts
+++ b/test/presets/vercel.test.ts
@@ -103,6 +103,18 @@ describe("nitro:preset:vercel", async () => {
           {
             "handle": "filesystem",
           },
+          {
+            "dest": "/__nitro",
+            "src": "/rules/_/cached/noncached",
+          },
+          {
+            "dest": "/__nitro",
+            "src": "(?<url>/rules/_/noncached/.*)",
+          },
+          {
+            "dest": "/__nitro--rules---cached?url=$url",
+            "src": "(?<url>/rules/_/cached/.*)",
+          },
           {
             "dest": "/__nitro",
             "src": "/rules/dynamic",
diff --git a/test/tests.ts b/test/tests.ts
index 2d3744cf38..9e79185a38 100644
--- a/test/tests.ts
+++ b/test/tests.ts
@@ -57,6 +57,10 @@ export async function setupTest(preset: string) {
       },
       "/rules/nested/**": { redirect: "/base", headers: { "x-test": "test" } },
       "/rules/nested/override": { redirect: { to: "/other" } },
+      "/rules/_/noncached/cached": { swr: true },
+      "/rules/_/noncached/**": { swr: false, cache: false },
+      "/rules/_/cached/noncached": { cache: false, swr: false },
+      "/rules/_/cached/**": { swr: true },
     },
     timing: preset !== "cloudflare" && preset !== "vercel-edge",
   }));