diff --git a/lib/internal/modules/esm/translators.js b/lib/internal/modules/esm/translators.js
index e3baaaefa6c0..1a7840e96dc5 100644
--- a/lib/internal/modules/esm/translators.js
+++ b/lib/internal/modules/esm/translators.js
@@ -129,19 +129,32 @@ function loadCJSModuleWithSpecialRequire(module, source, url, filename, isMain,
     let importAttributes = kEmptyObject;
     if (!StringPrototypeStartsWith(specifier, 'node:') && !BuiltinModule.normalizeRequirableId(specifier)) {
       // TODO: do not depend on the monkey-patchable CJS loader here.
-      const path = CJSModule._resolveFilename(specifier, module);
-      switch (extname(path)) {
-        case '.json':
-          importAttributes = { __proto__: null, type: 'json' };
-          break;
-        case '.node':
-          // If it gets here in the translators, the hooks must have already been invoked
-          // in the loader. Skip them in the synthetic module evaluation step.
-          return wrapModuleLoad(specifier, module, false, kShouldSkipModuleHooks);
-        default:
-            // fall through
+      // The CJS resolver works on file paths, so it cannot resolve a specifier whose
+      // referrer is not a file - that happens when the source of this module comes from
+      // a load hook that gave it a non-file URL. Leave the specifier alone in that case
+      // and let the ESM resolver below run the hooks on it.
+      let path;
+      try {
+        path = CJSModule._resolveFilename(specifier, module);
+      } catch (err) {
+        if (err?.code !== 'MODULE_NOT_FOUND' || StringPrototypeStartsWith(url, 'file:')) {
+          throw err;
+        }
+      }
+      if (path !== undefined) {
+        switch (extname(path)) {
+          case '.json':
+            importAttributes = { __proto__: null, type: 'json' };
+            break;
+          case '.node':
+            // If it gets here in the translators, the hooks must have already been invoked
+            // in the loader. Skip them in the synthetic module evaluation step.
+            return wrapModuleLoad(specifier, module, false, kShouldSkipModuleHooks);
+          default:
+              // fall through
+        }
+        specifier = `${pathToFileURL(path)}`;
       }
-      specifier = `${pathToFileURL(path)}`;
     }
 
     // NOTE: This re-invented require() is only used on the loader-hook worker thread.
diff --git a/test/es-module/test-esm-loader-cjs-source-relative-require.mjs b/test/es-module/test-esm-loader-cjs-source-relative-require.mjs
new file mode 100644
index 000000000000..1ba64c9f704f
--- /dev/null
+++ b/test/es-module/test-esm-loader-cjs-source-relative-require.mjs
@@ -0,0 +1,17 @@
+// Flags: --experimental-loader ./test/fixtures/es-module-loaders/non-file-cjs-source.mjs
+import '../common/index.mjs';
+import assert from 'node:assert';
+
+// When a load hook provides the source of a CommonJS module, the `require` calls
+// that source makes are resolved by the ESM loader, so registered hooks apply to
+// them. That has to keep working when the module has a URL that is not a file:
+// the CJS resolver cannot resolve a relative specifier against such a referrer.
+
+const { default: fromHookedRequire } = await import('custom:entry');
+assert.strictEqual(fromHookedRequire, 'loaded through the hooks');
+
+// When the hooks do not claim the specifier either, the failure has to come from
+// the ESM resolver rather than from the CJS one.
+await assert.rejects(import('custom:missing-dep'), {
+  code: 'ERR_UNSUPPORTED_RESOLVE_REQUEST',
+});
diff --git a/test/fixtures/es-module-loaders/non-file-cjs-source.mjs b/test/fixtures/es-module-loaders/non-file-cjs-source.mjs
new file mode 100644
index 000000000000..7436e7e30fd4
--- /dev/null
+++ b/test/fixtures/es-module-loaders/non-file-cjs-source.mjs
@@ -0,0 +1,25 @@
+// Serves CommonJS sources under a non-file URL scheme, so that the `require`
+// calls they contain have a referrer that the CJS resolver cannot handle.
+
+const sources = {
+  'custom:entry': 'module.exports = require("./dep");',
+  'custom:dep': 'module.exports = "loaded through the hooks";',
+  'custom:missing-dep': 'module.exports = require("./no-such-dep");',
+};
+
+export function resolve(specifier, context, next) {
+  if (specifier in sources) {
+    return { shortCircuit: true, url: specifier };
+  }
+  if (specifier === './dep') {
+    return { shortCircuit: true, url: 'custom:dep' };
+  }
+  return next(specifier, context);
+}
+
+export function load(url, context, next) {
+  if (url in sources) {
+    return { shortCircuit: true, format: 'commonjs', source: sources[url] };
+  }
+  return next(url, context);
+}