diff --git a/packages/base/card-serialization.ts b/packages/base/card-serialization.ts
index becd3af72c..167717366a 100644
--- a/packages/base/card-serialization.ts
+++ b/packages/base/card-serialization.ts
@@ -28,6 +28,7 @@ import {
   getSerializer,
   humanReadable,
   identifyCard,
+  isRegisteredPrefix,
   isSingleCardDocument,
   isSingleFileMetaDocument,
   loadCardDef,
@@ -221,6 +222,11 @@ export function serializeCard(
     ...opts,
     ...{
       maybeRelativeURL(possibleURL: string) {
+        // Registered prefix refs (e.g. @cardstack/catalog/foo) are already
+        // in their canonical portable form — return as-is
+        if (isRegisteredPrefix(possibleURL)) {
+          return possibleURL;
+        }
         let url = maybeURL(possibleURL, modelRelativeTo);
         if (!url) {
           throw new Error(
@@ -316,6 +322,11 @@ export function serializeFileDef(
       ...opts,
       ...{
         maybeRelativeURL(possibleURL: string) {
+          // Registered prefix refs (e.g. @cardstack/catalog/foo) are already
+          // in their canonical portable form — return as-is
+          if (isRegisteredPrefix(possibleURL)) {
+            return possibleURL;
+          }
           let url = maybeURL(possibleURL, modelRelativeTo);
           if (!url) {
             throw new Error(
diff --git a/packages/runtime-common/card-reference-resolver.ts b/packages/runtime-common/card-reference-resolver.ts
index ac1ae601f2..b6ed6cad73 100644
--- a/packages/runtime-common/card-reference-resolver.ts
+++ b/packages/runtime-common/card-reference-resolver.ts
@@ -7,6 +7,15 @@ export function registerCardReferencePrefix(
   prefixMappings.set(prefix, targetURL);
 }
 
+export function isRegisteredPrefix(reference: string): boolean {
+  for (let [prefix] of prefixMappings) {
+    if (reference.startsWith(prefix)) {
+      return true;
+    }
+  }
+  return false;
+}
+
 function isUrlLikeReference(ref: string): boolean {
   return (
     ref.startsWith('.') ||
@@ -32,3 +41,15 @@ export function resolveCardReference(
   }
   return new URL(reference, relativeTo).href;
 }
+
+// Reverse of resolveCardReference: converts a resolved URL back to
+// its registered prefix form if one matches.
+// e.g. "http://localhost:4201/catalog/foo" → "@cardstack/catalog/foo"
+export function unresolveCardReference(resolvedURL: string): string {
+  for (let [prefix, target] of prefixMappings) {
+    if (resolvedURL.startsWith(target)) {
+      return prefix + resolvedURL.slice(target.length);
+    }
+  }
+  return resolvedURL;
+}
diff --git a/packages/runtime-common/definition-lookup.ts b/packages/runtime-common/definition-lookup.ts
index 3a5d3a975c..ef3f9c1b91 100644
--- a/packages/runtime-common/definition-lookup.ts
+++ b/packages/runtime-common/definition-lookup.ts
@@ -25,7 +25,9 @@ import {
   hasExecutableExtension,
   trimExecutableExtension,
 } from './index';
+import { isRegisteredPrefix } from './card-reference-resolver';
 import type { VirtualNetwork } from './virtual-network';
+import { unresolveCardReference } from './card-reference-resolver';
 
 const MODULES_TABLE = 'modules';
 const PREFERRED_EXECUTABLE_EXTENSIONS = ['.gts', '.ts', '.gjs', '.js'];
@@ -40,7 +42,7 @@ function canonicalURL(url: string, relativeTo?: string): string {
     let parsed = new URL(url, relativeTo);
     parsed.search = '';
     parsed.hash = '';
-    return parsed.href;
+    return unresolveCardReference(parsed.href);
   } catch (_e) {
     let stripped = url.split('#')[0] ?? url;
     return stripped.split('?')[0] ?? stripped;
@@ -54,7 +56,8 @@ function normalizeExecutableURL(url: string): string {
   try {
     return trimExecutableExtension(new URL(url)).href;
   } catch (_e) {
-    return url;
+    // Handle non-URL identifiers like @cardstack/catalog/foo.gts
+    return url.replace(/\.(gts|ts|js|gjs)$/, '');
   }
 }
 
@@ -769,6 +772,11 @@ export class CachingDefinitionLookup implements DefinitionLookup {
 
   private normalizeDependencyForLookup(dep: string, relativeTo: URL): string {
     let canonical = canonicalURL(dep, relativeTo.href);
+    // For registered prefix deps (e.g. @cardstack/catalog/foo.gts),
+    // trim executable extensions without URL parsing
+    if (isRegisteredPrefix(canonical)) {
+      return canonical.replace(/\.(gts|ts|js|gjs)$/, '');
+    }
     try {
       let url = new URL(canonical);
       if (hasExecutableExtension(url.href)) {
diff --git a/packages/runtime-common/index-runner/dependency-normalization.ts b/packages/runtime-common/index-runner/dependency-normalization.ts
index 840f673eb0..ff7a340065 100644
--- a/packages/runtime-common/index-runner/dependency-normalization.ts
+++ b/packages/runtime-common/index-runner/dependency-normalization.ts
@@ -1,4 +1,5 @@
 import { trimExecutableExtension } from '../index';
+import { isRegisteredPrefix } from '../card-reference-resolver';
 import { canonicalURL } from './dependency-url';
 
 export function isExtensionlessPath(url: URL): boolean {
@@ -53,6 +54,11 @@ export function normalizeDependencyForLookup(
   relativeTo: URL,
 ): string {
   let canonical = canonicalURL(dep, relativeTo.href);
+  // For registered prefix deps (e.g. @cardstack/catalog/foo.gts),
+  // trim executable extensions without URL parsing
+  if (isRegisteredPrefix(canonical)) {
+    return canonical.replace(/\.(gts|ts|js|gjs)$/, '');
+  }
   try {
     return trimExecutableExtension(new URL(canonical)).href;
   } catch (_err) {
diff --git a/packages/runtime-common/index-runner/dependency-url.ts b/packages/runtime-common/index-runner/dependency-url.ts
index 1ba232786e..813d76e4e4 100644
--- a/packages/runtime-common/index-runner/dependency-url.ts
+++ b/packages/runtime-common/index-runner/dependency-url.ts
@@ -1,12 +1,23 @@
-import { resolveCardReference } from '../card-reference-resolver';
+import {
+  resolveCardReference,
+  unresolveCardReference,
+  isRegisteredPrefix,
+} from '../card-reference-resolver';
 
 export function canonicalURL(url: string, relativeTo?: string): string {
   try {
+    // If the URL is already a registered prefix (e.g. @cardstack/catalog/foo),
+    // keep it in that form — it's already canonical.
+    if (isRegisteredPrefix(url)) {
+      let stripped = url.split('#')[0] ?? url;
+      return stripped.split('?')[0] ?? stripped;
+    }
     let resolved = resolveCardReference(url, relativeTo);
     let parsed = new URL(resolved);
     parsed.search = '';
     parsed.hash = '';
-    return parsed.href;
+    // Convert resolved URLs back to prefix form if possible
+    return unresolveCardReference(parsed.href);
   } catch (_e) {
     let stripped = url.split('#')[0] ?? url;
     return stripped.split('?')[0] ?? stripped;
diff --git a/packages/runtime-common/index.ts b/packages/runtime-common/index.ts
index a1df4bef82..2b9b472293 100644
--- a/packages/runtime-common/index.ts
+++ b/packages/runtime-common/index.ts
@@ -222,7 +222,10 @@ export { v4 as uuidv4 } from '@lukeed/uuid'; // isomorphic UUID's using Math.ran
 import type { LocalPath } from './paths';
 import type { CardTypeFilter, Query, DataQuery, EveryFilter } from './query';
 import { Loader } from './loader';
-import { resolveCardReference } from './card-reference-resolver';
+import {
+  resolveCardReference,
+  unresolveCardReference,
+} from './card-reference-resolver';
 export * from './paths';
 export * from './cached-fetch';
 export * from './definition-lookup';
@@ -664,9 +667,11 @@ export function internalKeyFor(
   relativeTo: URL | undefined,
 ): string {
   if (!('type' in ref)) {
-    let module = trimExecutableExtension(
-      new URL(resolveCardReference(ref.module, relativeTo)),
-    ).href;
+    let resolved = resolveCardReference(ref.module, relativeTo);
+    let module = trimExecutableExtension(new URL(resolved)).href;
+    // Use the prefix form (e.g. @cardstack/catalog/foo) as the canonical
+    // internal key when a registered prefix mapping matches
+    module = unresolveCardReference(module);
     return `${module}/${ref.name}`;
   }
   switch (ref.type) {
diff --git a/packages/runtime-common/loader.ts b/packages/runtime-common/loader.ts
index 2f73200628..217ac1d8cb 100644
--- a/packages/runtime-common/loader.ts
+++ b/packages/runtime-common/loader.ts
@@ -10,6 +10,7 @@ import {
   trackRuntimeModuleDependency,
   type RuntimeDependencyTrackingContext,
 } from './dependency-tracker';
+import { unresolveCardReference } from './card-reference-resolver';
 
 type FetchingModule = {
   state: 'fetching';
@@ -562,7 +563,9 @@ export class Loader {
     module: any,
     moduleIdentifier: string,
   ) {
-    let moduleId = trimExecutableExtension(new URL(moduleIdentifier)).href;
+    let moduleId = unresolveCardReference(
+      trimExecutableExtension(new URL(moduleIdentifier)).href,
+    );
     for (let propName of Object.keys(module)) {
       let exportedEntity = module[propName];
       if (
diff --git a/packages/runtime-common/realm-index-query-engine.ts b/packages/runtime-common/realm-index-query-engine.ts
index 23bbd8f6c7..fc61c1d811 100644
--- a/packages/runtime-common/realm-index-query-engine.ts
+++ b/packages/runtime-common/realm-index-query-engine.ts
@@ -9,6 +9,7 @@ import {
   maxLinkDepth,
   maybeURL,
   resolveCardReference,
+  isRegisteredPrefix,
   IndexQueryEngine,
   codeRefWithAbsoluteURL,
   logger,
@@ -1038,6 +1039,11 @@ function relativizeResource(
     setURL(maybeRelativeURL(urlObj, primaryURL, realmURL));
   });
   visitModuleDeps(resource, (moduleURL, setModuleURL) => {
+    // Registered prefix references (e.g. @cardstack/catalog/foo) are already
+    // in their canonical portable form — don't resolve or relativize them.
+    if (isRegisteredPrefix(moduleURL)) {
+      return;
+    }
     let absoluteModuleURL = new URL(
       resolveCardReference(moduleURL, resource.id ?? primaryURL),
     );