diff --git a/common/changes/@microsoft/rush/resolver-cache-cache_2025-08-25-20-30.json b/common/changes/@microsoft/rush/resolver-cache-cache_2025-08-25-20-30.json
new file mode 100644
index 00000000000..d0c66e2eb49
--- /dev/null
+++ b/common/changes/@microsoft/rush/resolver-cache-cache_2025-08-25-20-30.json
@@ -0,0 +1,10 @@
+{
+  "changes": [
+    {
+      "packageName": "@microsoft/rush",
+      "comment": "[resolver-cache-plugin] Optimize search for nested package.json files with persistent cache file keyed by integrity hash.",
+      "type": "none"
+    }
+  ],
+  "packageName": "@microsoft/rush"
+}
\ No newline at end of file
diff --git a/rush-plugins/rush-resolver-cache-plugin/src/afterInstallAsync.ts b/rush-plugins/rush-resolver-cache-plugin/src/afterInstallAsync.ts
index 5917bb1a5d5..118159e5601 100644
--- a/rush-plugins/rush-resolver-cache-plugin/src/afterInstallAsync.ts
+++ b/rush-plugins/rush-resolver-cache-plugin/src/afterInstallAsync.ts
@@ -42,6 +42,10 @@ function getPlatformInfo(): IPlatformInfo {
 
 const END_TOKEN: string = '/package.json":';
 
+interface INestedPackageJsonCache {
+  subPackagesByIntegrity: [string, string[] | boolean][];
+}
+
 /**
  * Plugin entry point for after install.
  * @param rushSession - The Rush Session
@@ -80,9 +84,21 @@ export async function afterInstallAsync(
     rushConfiguration.getProjectLookupForRoot(workspaceRoot);
 
   const cacheFilePath: string = `${workspaceRoot}/resolver-cache.json`;
+  const subPackageCacheFilePath: string = `${workspaceRoot}/subpackage-entry-cache.json`;
 
   terminal.writeLine(`Resolver cache will be written at ${cacheFilePath}`);
 
+  let oldSubPackagesByIntegrity: Map<string, string[] | boolean> | undefined;
+  const subPackagesByIntegrity: Map<string, string[] | boolean> = new Map();
+  try {
+    const cacheContent: string = await FileSystem.readFileAsync(subPackageCacheFilePath);
+    const cacheJson: INestedPackageJsonCache = JSON.parse(cacheContent);
+    oldSubPackagesByIntegrity = new Map(cacheJson.subPackagesByIntegrity);
+    terminal.writeLine(`Loaded subpackage cache from ${subPackageCacheFilePath}`);
+  } catch (err) {
+    // Ignore
+  }
+
   async function afterExternalPackagesAsync(
     contexts: Map<string, IResolverContext>,
     missingOptionalDependencies: Set<string>
@@ -91,9 +107,11 @@ export async function afterInstallAsync(
      * Loads the index file from the pnpm store to discover nested package.json files in an external package
      * For internal packages, assumes there are no nested package.json files.
      * @param context - The context to find nested package.json files for
-     * @returns A promise that resolves when the nested package.json files are found, if applicable
+     * @returns A promise that resolves to the nested package.json paths, false if the package fails to load, or true if the package has no nested package.json files.
      */
-    async function findNestedPackageJsonsForContextAsync(context: IResolverContext): Promise<void> {
+    async function tryFindNestedPackageJsonsForContextAsync(
+      context: IResolverContext
+    ): Promise<string[] | boolean> {
       const { descriptionFileRoot, descriptionFileHash } = context;
 
       if (descriptionFileHash === undefined) {
@@ -101,7 +119,7 @@ export async function afterInstallAsync(
         terminal.writeDebugLine(
           `Package at ${descriptionFileRoot} does not have a file list. Assuming no nested "package.json" files.`
         );
-        return;
+        return true;
       }
 
       // Convert an integrity hash like
@@ -121,8 +139,6 @@ export async function afterInstallAsync(
         let endIndex: number = indexContent.lastIndexOf(END_TOKEN);
         if (endIndex > 0) {
           const nestedPackageDirs: string[] = [];
-          // eslint-disable-next-line require-atomic-updates
-          context.nestedPackageDirs = nestedPackageDirs;
           do {
             const startIndex: number = indexContent.lastIndexOf('"', endIndex);
             if (startIndex < 0) {
@@ -134,17 +150,54 @@ export async function afterInstallAsync(
             nestedPackageDirs.push(nestedPath);
             endIndex = indexContent.lastIndexOf(END_TOKEN, startIndex - 1);
           } while (endIndex > 0);
+          return nestedPackageDirs;
         }
+        return true;
       } catch (error) {
         if (!context.optional) {
           throw new Error(
             `Error reading index file for: "${context.descriptionFileRoot}" (${descriptionFileHash}): ${error.toString()}`
           );
-        } else {
-          terminal.writeLine(`Trimming missing optional dependency at: ${descriptionFileRoot}`);
-          contexts.delete(descriptionFileRoot);
-          missingOptionalDependencies.add(descriptionFileRoot);
         }
+        return false;
+      }
+    }
+    /**
+     * Loads the index file from the pnpm store to discover nested package.json files in an external package
+     * For internal packages, assumes there are no nested package.json files.
+     * @param context - The context to find nested package.json files for
+     * @returns A promise that resolves when the nested package.json files are found, if applicable
+     */
+    async function findNestedPackageJsonsForContextAsync(context: IResolverContext): Promise<void> {
+      const { descriptionFileRoot, descriptionFileHash } = context;
+
+      if (descriptionFileHash === undefined) {
+        // Assume this package has no nested package json files for now.
+        terminal.writeDebugLine(
+          `Package at ${descriptionFileRoot} does not have a file list. Assuming no nested "package.json" files.`
+        );
+        return;
+      }
+
+      let result: string[] | boolean | undefined =
+        oldSubPackagesByIntegrity?.get(descriptionFileHash) ??
+        subPackagesByIntegrity.get(descriptionFileHash);
+      if (result === undefined) {
+        result = await tryFindNestedPackageJsonsForContextAsync(context);
+      }
+      subPackagesByIntegrity.set(descriptionFileHash, result);
+      if (result === true) {
+        // Default case. Do nothing.
+      } else if (result === false) {
+        terminal.writeLine(`Trimming missing optional dependency at: ${descriptionFileRoot}`);
+        contexts.delete(descriptionFileRoot);
+        missingOptionalDependencies.add(descriptionFileRoot);
+      } else {
+        terminal.writeDebugLine(
+          `Nested "package.json" files found for package at ${descriptionFileRoot}: ${result.join(', ')}`
+        );
+        // eslint-disable-next-line require-atomic-updates
+        context.nestedPackageDirs = result;
       }
     }
 
@@ -165,11 +218,20 @@ export async function afterInstallAsync(
     afterExternalPackagesAsync
   });
 
+  const newSubPackageCache: string = JSON.stringify({
+    subPackagesByIntegrity: Array.from(subPackagesByIntegrity)
+  });
+
   const serialized: string = JSON.stringify(cacheFile);
 
-  await FileSystem.writeFileAsync(cacheFilePath, serialized, {
-    ensureFolderExists: true
-  });
+  await Promise.all([
+    FileSystem.writeFileAsync(cacheFilePath, serialized, {
+      ensureFolderExists: true
+    }),
+    FileSystem.writeFileAsync(subPackageCacheFilePath, newSubPackageCache, {
+      ensureFolderExists: true
+    })
+  ]);
 
   terminal.writeLine(`Resolver cache written.`);
 }