diff --git a/ui/app/services/capabilities.ts b/ui/app/services/capabilities.ts
index c6cb36e274..c7ec786b87 100644
--- a/ui/app/services/capabilities.ts
+++ b/ui/app/services/capabilities.ts
@@ -12,11 +12,44 @@ import type ApiService from 'vault/services/api';
 import type NamespaceService from 'vault/services/namespace';
 import type { Capabilities, CapabilitiesMap, CapabilitiesData, CapabilityTypes } from 'vault/app-types';
 
+type CapabilityFetchOptions = {
+  routeForCache?: string;
+};
+
 export default class CapabilitiesService extends Service {
   @service declare readonly api: ApiService;
   @service declare readonly namespace: NamespaceService;
 
-  @tracked requestedPaths = new Set<string>([]);
+  /*
+   * API path caching for <CodeGeneratorPolicyFlyout />
+   * Cache API paths when capabilities are fetched during route model hooks
+   * so the flyout can prefill with relevant policy paths.
+   */
+  @tracked routePathCache = new Map<string, Set<string>>();
+
+  // Cache API paths requested for a particular route
+  cacheRoutePaths(route: string, apiPaths: string[]) {
+    this.routePathCache.set(route, new Set(apiPaths));
+  }
+
+  // Lookup the paths for a route. Returns exact match first then falls back to longest matching route prefix.
+  lookupRoutePaths(route: string) {
+    const exactMatch = this.routePathCache.get(route);
+    if (exactMatch) {
+      return exactMatch;
+    }
+
+    const routes = Array.from(this.routePathCache.keys());
+    const matchingRoutes = routes.filter((r) => route.includes(r));
+    if (matchingRoutes.length) {
+      // Return longest matching cached route which is the most specific parent
+      const bestMatch = matchingRoutes.reduce((a, b) => (a.length > b.length ? a : b), '');
+      return this.routePathCache.get(bestMatch);
+    }
+
+    return null;
+  }
+  /* End logic for <CodeGeneratorPolicyFlyout /> API path caching */
 
   /*
   Add API paths to the PATH_MAP constant using a friendly key, e.g. 'syncDestinations'.
@@ -33,6 +66,10 @@ export default class CapabilitiesService extends Service {
     return path(params || {});
   }
 
+  pathsForList(paths: (keyof typeof PATH_MAP)[], params: object) {
+    return paths.map((path) => this.pathFor(path, params));
+  }
+
   /*
   Users don't always have access to the capabilities-self endpoint in the current namespace.
   This can happen when logging in to a namespace and then navigating to a child namespace.
@@ -85,8 +122,11 @@ export default class CapabilitiesService extends Service {
     }, {});
   }
 
-  async fetch(paths: string[]): Promise<CapabilitiesMap> {
-    this.requestedPaths = new Set(paths);
+  async fetch(paths: string[], fetchOptions: CapabilityFetchOptions = {}): Promise<CapabilitiesMap> {
+    // Cache API paths if route name provided
+    if (fetchOptions?.routeForCache) {
+      this.cacheRoutePaths(fetchOptions.routeForCache, paths);
+    }
 
     const payload = { paths: paths.map((path) => this.relativeNamespacePath(path)) };
 
@@ -116,16 +156,16 @@ export default class CapabilitiesService extends Service {
 
   // convenience method for fetching capabilities for a singular path without needing to use pathFor
   // ex: capabilities.for('syncDestinations', { type: 'github', name: 'org-sync' });
-  async for<T>(key: keyof typeof PATH_MAP, params?: T) {
+  async for<T>(key: keyof typeof PATH_MAP, params?: T, fetchOptions: CapabilityFetchOptions = {}) {
     const path = this.pathFor(key, params);
-    return this.fetchPathCapabilities(path);
+    return this.fetchPathCapabilities(path, fetchOptions);
   }
 
   /*
   this method returns all of the capabilities for a singular path 
   */
-  async fetchPathCapabilities(path: string) {
-    const capabilities = await this.fetch([path]);
+  async fetchPathCapabilities(path: string, fetchOptions: CapabilityFetchOptions = {}) {
+    const capabilities = await this.fetch([path], fetchOptions);
     return capabilities[path] as Capabilities;
   }
 
diff --git a/ui/lib/core/addon/components/code-generator/policy/flyout.ts b/ui/lib/core/addon/components/code-generator/policy/flyout.ts
index ebc59c94ad..796729aa66 100644
--- a/ui/lib/core/addon/components/code-generator/policy/flyout.ts
+++ b/ui/lib/core/addon/components/code-generator/policy/flyout.ts
@@ -10,6 +10,7 @@ import { formatStanzas, policySnippetArgs, PolicyStanza } from 'core/utils/code-
 import { validate } from 'vault/utils/forms/validate';
 import { service } from '@ember/service';
 import { task } from 'ember-concurrency';
+import routerLookup from 'core/utils/router-lookup';
 
 import type { HTMLElementEvent } from 'vault/forms';
 import type { PolicyData } from './builder';
@@ -18,9 +19,11 @@ import type ApiService from 'vault/services/api';
 import type CapabilitiesService from 'vault/services/capabilities';
 import type FlashMessageService from 'ember-cli-flash/services/flash-messages';
 import type VersionService from 'vault/services/version';
+import type RouterService from '@ember/routing/router-service';
 
 interface Args {
   onClose?: CallableFunction;
+  policyPaths: string[];
 }
 
 export default class CodeGeneratorPolicyFlyout extends Component<Args> {
@@ -42,6 +45,10 @@ export default class CodeGeneratorPolicyFlyout extends Component<Args> {
   @tracked stanzas: PolicyStanza[] = this.defaultStanzas;
   @tracked validationErrors: ValidationMap | null = null;
 
+  get router(): RouterService {
+    return routerLookup(this);
+  }
+
   validationError = (param: string) => {
     const { isValid, errors } = this.validationErrors?.[param] ?? {};
     return !isValid && errors ? errors.join(' ') : '';
@@ -97,16 +104,14 @@ export default class CodeGeneratorPolicyFlyout extends Component<Args> {
   @action
   openFlyout() {
     this.showFlyout = true;
-    const presetStanzas = Array.from(this.capabilities.requestedPaths).map(
-      (path) => new PolicyStanza({ path })
-    );
 
     const defaultState = formatStanzas(this.defaultStanzas);
     const currentState = formatStanzas(this.stanzas);
     const noChanges = currentState === defaultState;
     // Only preset stanzas if no changes have been made to the flyout
-    if (presetStanzas.length && noChanges) {
-      this.stanzas = presetStanzas;
+    if (noChanges) {
+      const presetStanzas = this.computePolicyPaths();
+      this.stanzas = presetStanzas ? presetStanzas : this.stanzas;
     }
   }
 
@@ -127,4 +132,24 @@ export default class CodeGeneratorPolicyFlyout extends Component<Args> {
     this.policyContent = '';
     this.stanzas = [new PolicyStanza()];
   }
+
+  computePolicyPaths() {
+    // Explicit policy paths take precedence
+    if (this.args.policyPaths) {
+      return this.presetStanzas(this.args.policyPaths);
+    }
+
+    const currentRouteName = this.router.currentRouteName;
+    if (!currentRouteName) {
+      return null;
+    }
+
+    const routePolicyPaths = this.capabilities.lookupRoutePaths(currentRouteName);
+    return routePolicyPaths ? this.presetStanzas(Array.from(routePolicyPaths)) : null;
+  }
+
+  presetStanzas(paths: string[]) {
+    const presetStanzas = paths.map((path) => new PolicyStanza({ path }));
+    return presetStanzas.length ? presetStanzas : null;
+  }
 }
diff --git a/ui/lib/core/addon/components/linked-block.js b/ui/lib/core/addon/components/linked-block.js
index 04e30105d2..4d6b0e4542 100644
--- a/ui/lib/core/addon/components/linked-block.js
+++ b/ui/lib/core/addon/components/linked-block.js
@@ -4,9 +4,9 @@
  */
 
 import Component from '@glimmer/component';
-import { getOwner } from '@ember/owner';
 import { action } from '@ember/object';
 import { encodePath } from 'vault/utils/path-encoding-helpers';
+import routerLookup from 'core/utils/router-lookup';
 
 /**
  * @module LinkedBlock
@@ -26,13 +26,8 @@ import { encodePath } from 'vault/utils/path-encoding-helpers';
  */
 
 export default class LinkedBlockComponent extends Component {
-  // We don't import the router service here because Ember Engine's use the alias 'app-router'
-  // Since this component is shared across engines, we look up the router dynamically using getOwner instead.
-  // This way we avoid throwing an error by looking up a service that doesn't exist.
-  // https://guides.emberjs.com/release/services/#toc_accessing-services
   get router() {
-    const owner = getOwner(this);
-    return owner.lookup('service:router') || owner.lookup('service:app-router');
+    return routerLookup(this);
   }
 
   @action
diff --git a/ui/lib/core/addon/utils/router-lookup.ts b/ui/lib/core/addon/utils/router-lookup.ts
new file mode 100644
index 0000000000..cf29292f36
--- /dev/null
+++ b/ui/lib/core/addon/utils/router-lookup.ts
@@ -0,0 +1,20 @@
+/**
+ * Copyright IBM Corp. 2016, 2025
+ * SPDX-License-Identifier: BUSL-1.1
+ */
+
+import { getOwner } from '@ember/owner';
+
+import type RouterService from '@ember/routing/router-service';
+
+// In components shared across engines, we have to look up the router dynamically
+// and use getOwner because Ember Engine's use the alias 'app-router'.
+// This way we avoid throwing an error by looking up a service that doesn't exist.
+// https://guides.emberjs.com/release/services/#toc_accessing-services
+export default function routerLookup(context: object) {
+  const owner = getOwner(context);
+  return (
+    (owner?.lookup('service:router') as RouterService) ||
+    (owner?.lookup('service:app-router') as RouterService)
+  );
+}
diff --git a/ui/lib/kv/addon/routes/list-directory.js b/ui/lib/kv/addon/routes/list-directory.js
index dafa206ff0..f199d01e7b 100644
--- a/ui/lib/kv/addon/routes/list-directory.js
+++ b/ui/lib/kv/addon/routes/list-directory.js
@@ -57,7 +57,11 @@ export default class KvSecretsListRoute extends Route {
     const backend = this.secretMountPath.currentPath;
     const filterValue = pathToSecret ? (pageFilter ? pathToSecret + pageFilter : pathToSecret) : pageFilter;
     const secrets = await this.fetchMetadata(backend, pathToSecret, params);
-    const capabilities = await this.capabilities.for('kvMetadata', { backend, path: path_to_secret });
+    const capabilities = await this.capabilities.for(
+      'kvMetadata',
+      { backend, path: path_to_secret },
+      { routeForCache: 'vault.cluster.secrets.backend.kv' }
+    );
     const backendModel = this.modelFor('application');
 
     return {
diff --git a/ui/lib/kv/addon/routes/secret.js b/ui/lib/kv/addon/routes/secret.js
index a03ce71d44..7deea498d8 100644
--- a/ui/lib/kv/addon/routes/secret.js
+++ b/ui/lib/kv/addon/routes/secret.js
@@ -65,14 +65,10 @@ export default class KvSecretRoute extends Route {
     const undeletePath = `${backend}/undelete/${path}`;
     const destroyPath = `${backend}/destroy/${path}`;
 
-    const perms = await this.capabilities.fetch([
-      metadataPath,
-      dataPath,
-      subkeysPath,
-      deletePath,
-      undeletePath,
-      destroyPath,
-    ]);
+    const apiPaths = [metadataPath, dataPath, subkeysPath, deletePath, undeletePath, destroyPath];
+    const perms = await this.capabilities.fetch(apiPaths, {
+      routeForCache: 'vault.cluster.secrets.backend.kv.secret',
+    });
 
     return {
       canReadData: perms[dataPath].canRead,
diff --git a/ui/tests/integration/components/code-generator/policy/flyout-test.js b/ui/tests/integration/components/code-generator/policy/flyout-test.js
index fdc1e87dc8..59e517264e 100644
--- a/ui/tests/integration/components/code-generator/policy/flyout-test.js
+++ b/ui/tests/integration/components/code-generator/policy/flyout-test.js
@@ -25,6 +25,7 @@ module('Integration | Component | code-generator/policy/flyout', function (hooks
     this.version = this.owner.lookup('service:version');
     this.version.type = 'enterprise'; // the flyout is only available for enterprise versions
     this.onClose = undefined;
+    this.policyPaths = undefined;
     this.assertSaveRequest = (assert, expectedPolicy, msg = 'policy content is correct') => {
       this.server.post('/sys/policies/acl/:name', (_, req) => {
         const { policy } = JSON.parse(req.requestBody);
@@ -35,7 +36,9 @@ module('Integration | Component | code-generator/policy/flyout', function (hooks
       });
     };
     this.renderComponent = async ({ open = true } = {}) => {
-      await render(hbs`<CodeGenerator::Policy::Flyout @onClose={{this.onClose}} />`);
+      await render(
+        hbs`<CodeGenerator::Policy::Flyout @onClose={{this.onClose}} @policyPaths={{this.policyPaths}} />`
+      );
       if (open) {
         await click(GENERAL.button('Generate policy'));
       }
@@ -72,6 +75,20 @@ module('Integration | Component | code-generator/policy/flyout', function (hooks
     assert.dom(GENERAL.flyout).doesNotExist('flyout closes after clicking cancel');
   });
 
+  test('it presets with paths from @policyPaths array', async function (assert) {
+    this.policyPaths = ['some/preset/path'];
+    await this.renderComponent();
+    assert.dom(SELECTORS.pathByContainer(0)).hasValue('some/preset/path');
+    assert.dom(GENERAL.cardContainer()).exists({ count: 1 });
+  });
+
+  test('it handles empty @policyPaths array', async function (assert) {
+    this.policyPaths = [];
+    await this.renderComponent();
+
+    assert.dom(SELECTORS.pathByContainer(0)).hasValue('', 'does not prepopulate with empty array');
+  });
+
   test('it yields custom trigger component', async function (assert) {
     await render(hbs`<Hds::Dropdown as |D|>
       <D.ToggleButton @text="Toolbox" data-test-dropdown="Toolbox" />
@@ -346,83 +363,138 @@ EOT`;
     assert.dom(GENERAL.validationErrorByAttr('name')).doesNotExist('validation error is cleared');
   });
 
-  module('capabilities', function (hooks) {
+  module('capabilities service prepopulating', function (hooks) {
     hooks.beforeEach(function () {
       this.capabilities = this.owner.lookup('service:capabilities');
+      const router = this.owner.lookup('service:router');
+      this.currentRouteNameStub = Sinon.stub(router, 'currentRouteName');
+      this.cacheCapabilityPaths = (route, paths) => {
+        this.capabilities.cacheRoutePaths(route, paths);
+      };
     });
 
-    test('it renders when no capabilities have been requested', async function (assert) {
-      this.capabilities.requestedPaths = new Set([]);
+    hooks.afterEach(function () {
+      this.currentRouteNameStub.restore();
+    });
+
+    test('it handles null currentRouteName gracefully', async function (assert) {
+      this.currentRouteNameStub.value(null);
+      await this.renderComponent();
+      assert.dom(SELECTORS.pathByContainer(0)).hasValue('', 'does not prepopulate when route name is null');
+      assert.dom(GENERAL.cardContainer()).exists({ count: 1 });
+    });
+
+    test('it does not prepopulate when no paths have been cached', async function (assert) {
       await this.renderComponent();
       assert.dom(SELECTORS.pathByContainer(0)).hasValue('');
     });
 
-    test('it prepopulates with a single capability path', async function (assert) {
-      this.capabilities.requestedPaths = new Set(['super-secret/data']);
+    test('it does not prepopulate paths when cached capabilities route is unrelated to the current route', async function (assert) {
+      this.currentRouteNameStub.value('vault.cluster.secrets.secret');
+      this.cacheCapabilityPaths('vault.cluster.settings', ['some/settings']);
+      await this.renderComponent();
+      assert.dom(SELECTORS.pathByContainer(0)).hasValue('');
+    });
+
+    test('it prepopulates paths when cached capabilities route equals current route', async function (assert) {
+      this.currentRouteNameStub.value('vault.cluster.secrets.secret');
+      this.cacheCapabilityPaths('vault.cluster.secrets.secret', ['super-secret/data']);
       await this.renderComponent();
       assert.dom(SELECTORS.pathByContainer(0)).hasValue('super-secret/data');
       assert.dom(GENERAL.cardContainer()).exists({ count: 1 });
     });
 
-    test('it prepopulates with a multiple capability paths', async function (assert) {
-      this.capabilities.requestedPaths = new Set(['path/one', 'path/two']);
+    test('it prepopulates paths from longest matching parent route', async function (assert) {
+      // Cache paths for parent route
+      this.cacheCapabilityPaths('vault.cluster.secrets.backend.kv.secret', [
+        'kv/data/my-secret',
+        'kv/metadata/my-secret',
+      ]);
+      this.cacheCapabilityPaths('vault.cluster.secrets.backend.kv', ['should/not/cache']);
+      // Current route is a child (e.g., secret.details)
+      this.currentRouteNameStub.value('vault.cluster.secrets.backend.kv.secret.details');
       await this.renderComponent();
-      assert.dom(SELECTORS.pathByContainer(0)).hasValue('path/one');
-      assert.dom(SELECTORS.pathByContainer(1)).hasValue('path/two');
+      assert.dom(SELECTORS.pathByContainer(0)).hasValue('kv/data/my-secret', 'uses parent paths');
+      assert.dom(SELECTORS.pathByContainer(1)).hasValue('kv/metadata/my-secret', 'includes all parent paths');
       assert.dom(GENERAL.cardContainer()).exists({ count: 2 });
     });
 
-    test('it does not override user changes to a preset path on reopen', async function (assert) {
-      this.capabilities.requestedPaths = new Set(['super-secret/data']);
-      await this.renderComponent();
+    // All of these tests run with the current route stubbed and cached paths
+    module('when the flyout is prepopulated', function (hooks) {
+      hooks.beforeEach(function () {
+        this.cacheCapabilityPaths('vault.cluster.secrets.secret', ['super-secret/data']);
+        this.currentRouteNameStub.value('vault.cluster.secrets.secret');
+      });
 
-      // User updates path
-      await typeIn(SELECTORS.pathByContainer(0), '/*');
-      // Close and reopen
-      await click(GENERAL.cancelButton);
-      await click(GENERAL.button('Generate policy'));
-      assert
-        .dom(SELECTORS.pathByContainer(0))
-        .hasValue('super-secret/data/*', 'user path changes are preserved');
-      assert.dom(GENERAL.cardContainer()).exists({ count: 1 });
-    });
+      test('paths from arg take precedence over capabilities service', async function (assert) {
+        this.policyPaths = ['super-explicit/path'];
+        await this.renderComponent();
+        assert.dom(SELECTORS.pathByContainer(0)).hasValue('super-explicit/path');
+        assert.dom(GENERAL.cardContainer()).exists({ count: 1 });
+      });
 
-    test('it does not override user capabilities selection for a preset path on reopen', async function (assert) {
-      this.capabilities.requestedPaths = new Set(['super-secret/data']);
-      await this.renderComponent();
+      test('it prepopulates with a single capability path', async function (assert) {
+        await this.renderComponent();
+        assert.dom(SELECTORS.pathByContainer(0)).hasValue('super-secret/data');
+        assert.dom(GENERAL.cardContainer()).exists({ count: 1 });
+      });
 
-      // User updates path
-      await click(SELECTORS.checkboxByContainer(0, 'read'));
-      // Close and reopen
-      await click(GENERAL.cancelButton);
-      await click(GENERAL.button('Generate policy'));
-      assert
-        .dom(SELECTORS.checkboxByContainer(0, 'read'))
-        .isChecked('user capabilities changes are preserved');
-      assert.dom(GENERAL.cardContainer()).exists({ count: 1 });
-    });
+      test('it prepopulates with multiple capability paths', async function (assert) {
+        this.cacheCapabilityPaths('vault.cluster.secrets.secret', ['path/one', 'path/two']);
+        await this.renderComponent();
+        assert.dom(SELECTORS.pathByContainer(0)).hasValue('path/one');
+        assert.dom(SELECTORS.pathByContainer(1)).hasValue('path/two');
+        assert.dom(GENERAL.cardContainer()).exists({ count: 2 });
+      });
 
-    test('it does not override user added stanza on reopen', async function (assert) {
-      this.capabilities.requestedPaths = new Set(['super-secret/data']);
-      await this.renderComponent();
-      await click(GENERAL.button('Add rule'));
-      await fillIn(SELECTORS.pathByContainer(1), 'new/path/*');
-      // Close and reopen
-      await click(GENERAL.cancelButton);
-      await click(GENERAL.button('Generate policy'));
-      assert.dom(GENERAL.cardContainer()).exists({ count: 2 }, 'it renders two stanzas after reopening');
-      assert.dom(SELECTORS.pathByContainer(0)).hasValue('super-secret/data', 'preset path still exists');
-      assert.dom(SELECTORS.pathByContainer(1)).hasValue('new/path/*', 'user added path still exists');
-    });
+      test('it does not override user changes to a preset path on reopen', async function (assert) {
+        await this.renderComponent();
+        // User updates path
+        await typeIn(SELECTORS.pathByContainer(0), '/*');
+        // Close and reopen
+        await click(GENERAL.cancelButton);
+        await click(GENERAL.button('Generate policy'));
+        assert
+          .dom(SELECTORS.pathByContainer(0))
+          .hasValue('super-secret/data/*', 'user path changes are preserved');
+        assert.dom(GENERAL.cardContainer()).exists({ count: 1 });
+      });
 
-    test('it does not save prepopulated paths as policy content', async function (assert) {
-      assert.expect(3);
-      this.capabilities.requestedPaths = new Set(['path/one', 'path/two']);
-      await this.renderComponent();
-      // Fill in name and save to make sure policyContent is empty
-      this.assertSaveRequest(assert, '', 'policy content is empty despite pre-filled paths');
-      await fillIn(GENERAL.inputByAttr('name'), 'test-policy');
-      await click(GENERAL.submitButton);
+      test('it does not override user capabilities selection for a preset path on reopen', async function (assert) {
+        await this.renderComponent();
+
+        // User updates path
+        await click(SELECTORS.checkboxByContainer(0, 'read'));
+        // Close and reopen
+        await click(GENERAL.cancelButton);
+        await click(GENERAL.button('Generate policy'));
+        assert
+          .dom(SELECTORS.checkboxByContainer(0, 'read'))
+          .isChecked('user capabilities changes are preserved');
+        assert.dom(GENERAL.cardContainer()).exists({ count: 1 });
+      });
+
+      test('it does not override user added stanza on reopen', async function (assert) {
+        await this.renderComponent();
+        await click(GENERAL.button('Add rule'));
+        await fillIn(SELECTORS.pathByContainer(1), 'new/path/*');
+        // Close and reopen
+        await click(GENERAL.cancelButton);
+        await click(GENERAL.button('Generate policy'));
+        assert.dom(GENERAL.cardContainer()).exists({ count: 2 }, 'it renders two stanzas after reopening');
+        assert.dom(SELECTORS.pathByContainer(0)).hasValue('super-secret/data', 'preset path still exists');
+        assert.dom(SELECTORS.pathByContainer(1)).hasValue('new/path/*', 'user added path still exists');
+      });
+
+      test('it does not save prepopulated paths as policy content', async function (assert) {
+        assert.expect(3);
+        this.cacheCapabilityPaths('vault.cluster.secrets.secret', ['path/one', 'path/two']);
+        await this.renderComponent();
+        // Fill in name and save to make sure policyContent is empty
+        this.assertSaveRequest(assert, '', 'policy content is empty despite pre-filled paths');
+        await fillIn(GENERAL.inputByAttr('name'), 'test-policy');
+        await click(GENERAL.submitButton);
+      });
     });
   });
 });
diff --git a/ui/tests/unit/services/capabilities-test.js b/ui/tests/unit/services/capabilities-test.js
index 8f29fdc408..38b901ed16 100644
--- a/ui/tests/unit/services/capabilities-test.js
+++ b/ui/tests/unit/services/capabilities-test.js
@@ -14,6 +14,7 @@ module('Unit | Service | capabilities', function (hooks) {
 
   hooks.beforeEach(function () {
     this.capabilities = this.owner.lookup('service:capabilities');
+    this.checkCachedPaths = (route) => this.capabilities.routePathCache.get(route);
     this.generateResponse = ({ path, paths, capabilities }) => {
       if (path) {
         // "capabilities" is an array
@@ -142,8 +143,9 @@ module('Unit | Service | capabilities', function (hooks) {
     assert.propEqual(actual, expected, `it returns expected response: ${JSON.stringify(actual)}`);
   });
 
-  test('fetch: it tracks the requested paths', async function (assert) {
+  test('fetch: it caches paths when routeForCache is provided', async function (assert) {
     const paths = ['/my/api/path', 'another/api/path'];
+    const route = 'vault.cluster.some-route';
 
     this.server.post('/sys/capabilities-self', () => {
       return this.generateResponse({
@@ -152,33 +154,110 @@ module('Unit | Service | capabilities', function (hooks) {
       });
     });
 
-    assert.strictEqual(this.capabilities.requestedPaths.size, 0, 'requestedPaths is empty before fetch');
-
-    await this.capabilities.fetch(paths);
-
-    assert.strictEqual(this.capabilities.requestedPaths.size, 2, 'requestedPaths contains 2 items');
-    assert.true(this.capabilities.requestedPaths.has('/my/api/path'), 'contains first path');
-    assert.true(this.capabilities.requestedPaths.has('another/api/path'), 'contains second path');
+    assert.strictEqual(this.capabilities.routePathCache.size, 0, 'cache is empty before fetch');
+    await this.capabilities.fetch(paths, { routeForCache: route });
+    assert.strictEqual(this.capabilities.routePathCache.size, 1, 'cache contains 1 route');
+    const cachedPaths = this.checkCachedPaths(route);
+    assert.deepEqual(Array.from(cachedPaths), paths, 'cached paths match fetched paths');
   });
 
-  test('fetch: it replaces requestedPaths on each call', async function (assert) {
-    const firstPaths = ['/path/one', '/path/two'];
-    const secondPaths = ['/path/three'];
-
+  test('fetch: it does not cache when routeForCache is not provided', async function (assert) {
+    const paths = ['/my/api/path'];
     this.server.post('/sys/capabilities-self', () => {
-      return this.generateResponse({
-        paths: firstPaths,
-        capabilities: { '/path/one': ['read'], '/path/two': ['read'], '/path/three': ['read'] },
-      });
+      return this.generateResponse({ paths, capabilities: { '/my/api/path': ['read'] } });
     });
+    await this.capabilities.fetch(paths);
+    assert.strictEqual(this.capabilities.routePathCache.size, 0, 'cache remains empty');
+  });
 
-    await this.capabilities.fetch(firstPaths);
-    assert.strictEqual(this.capabilities.requestedPaths.size, 2, 'initially has 2 paths');
+  test('cacheRoutePaths: it caches paths', async function (assert) {
+    const route = 'vault.cluster.some-route';
+    const apiPaths = ['/my/api/path', 'another/api/path'];
 
-    await this.capabilities.fetch(secondPaths);
-    assert.strictEqual(this.capabilities.requestedPaths.size, 1, 'updated to have 1 path');
-    assert.true(this.capabilities.requestedPaths.has('/path/three'), 'contains new path');
-    assert.false(this.capabilities.requestedPaths.has('/path/one'), 'no longer contains old path');
+    assert.strictEqual(this.capabilities.routePathCache.size, 0, 'routePathCache is empty before fetch');
+    this.capabilities.cacheRoutePaths(route, apiPaths);
+    assert.strictEqual(this.capabilities.routePathCache.size, 1, 'routePathCache contains 1 item');
+    const cachedPaths = this.checkCachedPaths(route);
+    assert.strictEqual(cachedPaths.size, 2, 'it stores 2 paths for the route');
+    assert.true(cachedPaths.has('/my/api/path'), 'contains first path');
+    assert.true(cachedPaths.has('another/api/path'), 'contains second path');
+  });
+
+  test('cacheRoutePaths: it caches the paths for multiple routes', async function (assert) {
+    const routeA = 'vault.cluster.route-A';
+    const pathsA = ['route/A/path'];
+    const routeB = 'vault.cluster.route-B';
+    const pathsB = ['route/B/path'];
+
+    this.capabilities.cacheRoutePaths(routeA, pathsA);
+    this.capabilities.cacheRoutePaths(routeB, pathsB);
+    assert.strictEqual(this.capabilities.routePathCache.size, 2, 'contains two items');
+    assert.true(this.checkCachedPaths(routeA).has(pathsA[0]), 'contains routeA path');
+    assert.true(this.checkCachedPaths(routeB).has(pathsB[0]), 'contains routeB path');
+  });
+
+  test('cacheRoutePaths: it replaces cached paths if called with the same route', async function (assert) {
+    const route = 'vault.cluster.some-route';
+    const firstCall = ['first/path'];
+
+    this.capabilities.cacheRoutePaths(route, firstCall);
+    const initialCache = this.checkCachedPaths(route);
+    assert.strictEqual(initialCache.size, 1, 'cached paths contains 1 path');
+    assert.true(initialCache.has(firstCall[0]), 'contains initial path');
+
+    const secondCall = ['second/path'];
+    this.capabilities.cacheRoutePaths(route, secondCall);
+    const secondCache = this.checkCachedPaths(route);
+    assert.strictEqual(secondCache.size, 1, 'second cache still contains 1 path');
+    assert.true(secondCache.has(secondCall[0]), 'path is from second call');
+  });
+
+  test('cacheRoutePaths: it deduplicates paths', async function (assert) {
+    const route = 'vault.cluster.some-route';
+    const paths = ['same/path', 'same/path', 'almost/same/path'];
+
+    this.capabilities.cacheRoutePaths(route, paths);
+    const cachedPaths = this.checkCachedPaths(route);
+    assert.strictEqual(cachedPaths.size, 2, 'routePathCache contains 2 items');
+    assert.true(cachedPaths.has('same/path'), 'contains first path');
+    assert.true(cachedPaths.has('almost/same/path'), 'contains second path');
+  });
+
+  test('lookupRoutePaths: it returns exact route match', async function (assert) {
+    const route = 'vault.cluster.some-route';
+    const pathSet = new Set(['apps/super-secret']);
+    this.capabilities.routePathCache.set(route, pathSet);
+
+    const returnedPaths = await this.capabilities.lookupRoutePaths(route);
+    assert.deepEqual(returnedPaths, pathSet, 'returned paths equal original set');
+  });
+
+  test('lookupRoutePaths: it returns longest matching route if multiple exist', async function (assert) {
+    const ancestor1 = 'vault.cluster.secrets';
+    const ancestor2 = 'vault.cluster.secrets.backend.kv';
+    const ancestor3 = 'vault.cluster.secrets.backend.kv.secret';
+    const pathSet1 = new Set(['apps/']);
+    const pathSet2 = new Set(['apps/github-creds/']);
+    const pathSet3 = new Set(['apps/github-creds/api-tokens']);
+    this.capabilities.routePathCache.set(ancestor1, pathSet1);
+    this.capabilities.routePathCache.set(ancestor2, pathSet2);
+    this.capabilities.routePathCache.set(ancestor3, pathSet3);
+
+    const returnedPaths = await this.capabilities.lookupRoutePaths(
+      'vault.cluster.secrets.backend.kv.secret.details'
+    );
+    assert.deepEqual(returnedPaths, pathSet3, 'it returns the paths that match the longest route');
+  });
+
+  test('lookupRoutePaths: it returns null when no routes are cached', async function (assert) {
+    const returnedPaths = await this.capabilities.lookupRoutePaths('vault.cluster.some-route');
+    assert.strictEqual(returnedPaths, null, 'returns null when cache is empty');
+  });
+
+  test('lookupRoutePaths: it returns null when no matching routes exist', async function (assert) {
+    this.capabilities.routePathCache.set('vault.cluster.secrets', new Set(['secret/']));
+    const returnedPaths = await this.capabilities.lookupRoutePaths('vault.cluster.settings.configure');
+    assert.strictEqual(returnedPaths, null, 'returns null when no routes match');
   });
 
   test('fetchPathCapabilities: it makes request to capabilities-self and returns capabilities for single path', async function (assert) {
@@ -221,6 +300,18 @@ module('Unit | Service | capabilities', function (hooks) {
     );
   });
 
+  test('pathsForList: it returns multiple PATH_MAP keys', async function (assert) {
+    const keys = ['kubernetesRole', 'kubernetesCreds'];
+    const params = { backend: 'k8', name: 'my-role' };
+    const paths = this.capabilities.pathsForList(keys, params);
+    assert.deepEqual(paths, ['k8/role/my-role', 'k8/creds/my-role'], 'computes all paths');
+  });
+
+  test('pathsForList: it handles an empty array', async function (assert) {
+    const paths = this.capabilities.pathsForList([], {});
+    assert.deepEqual(paths, [], 'returns empty array');
+  });
+
   test('for: it should fetch capabilities for single path using pathFor and fetchPathCapabilities methods', async function (assert) {
     const pathForStub = sinon.spy(this.capabilities, 'pathFor');
     const fetchPathCapabilitiesStub = sinon.stub(this.capabilities, 'fetchPathCapabilities').resolves();