diff --git a/packages/assets-controllers/CHANGELOG.md b/packages/assets-controllers/CHANGELOG.md
index 7bb393db474..12eaf6f79ed 100644
--- a/packages/assets-controllers/CHANGELOG.md
+++ b/packages/assets-controllers/CHANGELOG.md
@@ -7,9 +7,19 @@ and this project adheres to [Semantic Versioning](https://semver.org/spec/v2.0.0
 
 ## [Unreleased]
 
+### Added
+
+- Add dynamic fetching of supported networks from `/v2/supportedNetworks` API endpoint with fallback to hardcoded list ([#7716](https://github.com/MetaMask/core/pull/7716))
+  - Add `fetchSupportedNetworks()`, `getSupportedNetworks()`, and `resetSupportedNetworksCache()` exports from token-prices-service
+  - Add `setNativeAssetIdentifiers()` method to `CodefiTokenPricesServiceV2` for CAIP-19 native token lookups
+  - Add `updateSupportedNetworks()` method to `CodefiTokenPricesServiceV2`
+  - Add `NativeAssetIdentifiersMap` type export from token-prices-service
+- Integrate `TokenRatesController` with `NetworkEnablementController` to use native asset identifiers for token price lookups ([#7716](https://github.com/MetaMask/core/pull/7716))
+
 ### Changed
 
 - Bump `@metamask/keyring-controller` from `^25.0.0` to `^25.1.0` ([#7713](https://github.com/MetaMask/core/pull/7713))
+- Add `@metamask/network-enablement-controller` as a dependency ([#7716](https://github.com/MetaMask/core/pull/7716))
 
 ## [96.0.0]
 
diff --git a/packages/assets-controllers/package.json b/packages/assets-controllers/package.json
index 2957a493e2c..2f9bd216051 100644
--- a/packages/assets-controllers/package.json
+++ b/packages/assets-controllers/package.json
@@ -69,6 +69,7 @@
     "@metamask/metamask-eth-abis": "^3.1.1",
     "@metamask/multichain-account-service": "^5.1.0",
     "@metamask/network-controller": "^29.0.0",
+    "@metamask/network-enablement-controller": "^4.1.0",
     "@metamask/permission-controller": "^12.2.0",
     "@metamask/phishing-controller": "^16.1.0",
     "@metamask/polling-controller": "^16.0.2",
diff --git a/packages/assets-controllers/src/TokenRatesController.test.ts b/packages/assets-controllers/src/TokenRatesController.test.ts
index 2ab2ae504f9..761657d12dd 100644
--- a/packages/assets-controllers/src/TokenRatesController.test.ts
+++ b/packages/assets-controllers/src/TokenRatesController.test.ts
@@ -68,7 +68,11 @@ function buildTokenRatesControllerMessenger(
   });
   messenger.delegate({
     messenger: tokenRatesControllerMessenger,
-    actions: ['TokensController:getState', 'NetworkController:getState'],
+    actions: [
+      'TokensController:getState',
+      'NetworkController:getState',
+      'NetworkEnablementController:getState',
+    ],
     events: ['TokensController:stateChange', 'NetworkController:stateChange'],
   });
   return tokenRatesControllerMessenger;
@@ -83,6 +87,48 @@ describe('TokenRatesController', () => {
         });
       });
     });
+
+    it('should call setNativeAssetIdentifiers on tokenPricesService if available', async () => {
+      const setNativeAssetIdentifiers = jest.fn();
+      const tokenPricesService = buildMockTokenPricesService({
+        setNativeAssetIdentifiers,
+      });
+
+      await withController(
+        {
+          options: {
+            tokenPricesService,
+          },
+        },
+        async () => {
+          expect(setNativeAssetIdentifiers).toHaveBeenCalledWith({
+            'eip155:1': 'eip155:1/slip44:60',
+            'eip155:137': 'eip155:137/slip44:966',
+          });
+        },
+      );
+    });
+
+    it('should not fail if tokenPricesService does not have setNativeAssetIdentifiers', async () => {
+      const tokenPricesService = buildMockTokenPricesService();
+      // Explicitly remove setNativeAssetIdentifiers to simulate an old service
+      delete (tokenPricesService as Partial<AbstractTokenPricesService>)
+        .setNativeAssetIdentifiers;
+
+      await withController(
+        {
+          options: {
+            tokenPricesService,
+          },
+        },
+        async ({ controller }) => {
+          // Should not throw and controller should be created
+          expect(controller.state).toStrictEqual({
+            marketData: {},
+          });
+        },
+      );
+    });
   });
 
   describe('updateExchangeRates', () => {
@@ -1213,6 +1259,18 @@ async function withController<ReturnValue>(
     }),
   );
 
+  // Register NetworkEnablementController:getState handler
+  messenger.registerActionHandler(
+    'NetworkEnablementController:getState',
+    jest.fn().mockReturnValue({
+      enabledNetworkMap: {},
+      nativeAssetIdentifiers: {
+        'eip155:1': 'eip155:1/slip44:60',
+        'eip155:137': 'eip155:137/slip44:966',
+      },
+    }),
+  );
+
   const controller = new TokenRatesController({
     tokenPricesService: buildMockTokenPricesService(),
     messenger: buildTokenRatesControllerMessenger(messenger),
@@ -1259,6 +1317,7 @@ function buildMockTokenPricesService(
     validateCurrencySupported(_currency: unknown): _currency is string {
       return true;
     },
+    setNativeAssetIdentifiers: jest.fn(),
     ...overrides,
   };
 }
diff --git a/packages/assets-controllers/src/TokenRatesController.ts b/packages/assets-controllers/src/TokenRatesController.ts
index d4f7d002d4d..6b8df1e3f1c 100644
--- a/packages/assets-controllers/src/TokenRatesController.ts
+++ b/packages/assets-controllers/src/TokenRatesController.ts
@@ -9,6 +9,7 @@ import type {
   NetworkControllerGetStateAction,
   NetworkControllerStateChangeEvent,
 } from '@metamask/network-controller';
+import type { NetworkEnablementControllerGetStateAction } from '@metamask/network-enablement-controller';
 import { StaticIntervalPollingController } from '@metamask/polling-controller';
 import type { Hex } from '@metamask/utils';
 import { isEqual } from 'lodash';
@@ -93,7 +94,8 @@ type ChainIdAndNativeCurrency = {
  */
 export type AllowedActions =
   | TokensControllerGetStateAction
-  | NetworkControllerGetStateAction;
+  | NetworkControllerGetStateAction
+  | NetworkEnablementControllerGetStateAction;
 
 /**
  * The external events available to the {@link TokenRatesController}.
@@ -234,6 +236,9 @@ export class TokenRatesController extends StaticIntervalPollingController<TokenR
     this.#allTokens = allTokens;
     this.#allDetectedTokens = allDetectedTokens;
 
+    // Set native asset identifiers from NetworkEnablementController for CAIP-19 native token lookups
+    this.#initNativeAssetIdentifiers();
+
     this.#subscribeToTokensStateChange();
 
     this.#subscribeToNetworkStateChange();
@@ -317,6 +322,21 @@ export class TokenRatesController extends StaticIntervalPollingController<TokenR
     );
   }
 
+  /**
+   * Initialize the native asset identifiers from NetworkEnablementController.
+   * This provides CAIP-19 native asset IDs for the token prices service.
+   */
+  #initNativeAssetIdentifiers(): void {
+    if (this.#tokenPricesService.setNativeAssetIdentifiers) {
+      const { nativeAssetIdentifiers } = this.messenger.call(
+        'NetworkEnablementController:getState',
+      );
+      this.#tokenPricesService.setNativeAssetIdentifiers(
+        nativeAssetIdentifiers,
+      );
+    }
+  }
+
   /**
    * Get the tokens for the given chain.
    *
diff --git a/packages/assets-controllers/src/token-prices-service/abstract-token-prices-service.ts b/packages/assets-controllers/src/token-prices-service/abstract-token-prices-service.ts
index 22577107fa3..8c6ad9c9c85 100644
--- a/packages/assets-controllers/src/token-prices-service/abstract-token-prices-service.ts
+++ b/packages/assets-controllers/src/token-prices-service/abstract-token-prices-service.ts
@@ -1,8 +1,13 @@
 import type { ServicePolicy } from '@metamask/controller-utils';
-import type { CaipAssetType, Hex } from '@metamask/utils';
+import type { CaipAssetType, CaipChainId, Hex } from '@metamask/utils';
 
 import type { MarketDataDetails } from '../TokenRatesController';
 
+/**
+ * A map of CAIP-2 chain IDs to their native asset identifiers (CAIP-19 format).
+ */
+export type NativeAssetIdentifiersMap = Record<CaipChainId, CaipAssetType>;
+
 /**
  * Represents an exchange rate.
  */
@@ -103,4 +108,14 @@ export type AbstractTokenPricesService<
    * @returns True if the API supports the currency, false otherwise.
    */
   validateCurrencySupported(currency: unknown): currency is Currency;
+
+  /**
+   * Sets the native asset identifiers map for resolving native token CAIP-19 IDs.
+   * This should be called with data from NetworkEnablementController.state.nativeAssetIdentifiers.
+   *
+   * @param nativeAssetIdentifiers - Map of CAIP-2 chain IDs to native asset identifiers.
+   */
+  setNativeAssetIdentifiers?(
+    nativeAssetIdentifiers: NativeAssetIdentifiersMap,
+  ): void;
 };
diff --git a/packages/assets-controllers/src/token-prices-service/codefi-v2.test.ts b/packages/assets-controllers/src/token-prices-service/codefi-v2.test.ts
index bdb2c516e90..f00735fccd9 100644
--- a/packages/assets-controllers/src/token-prices-service/codefi-v2.test.ts
+++ b/packages/assets-controllers/src/token-prices-service/codefi-v2.test.ts
@@ -13,6 +13,9 @@ import {
   fetchSupportedCurrencies,
   getSupportedCurrencies,
   resetSupportedCurrenciesCache,
+  fetchSupportedNetworks,
+  getSupportedNetworks,
+  resetSupportedNetworksCache,
 } from './codefi-v2';
 
 // We're not customizing the default max delay
@@ -1920,6 +1923,237 @@ describe('CodefiTokenPricesServiceV2', () => {
       expect(result).toStrictEqual([...SUPPORTED_CURRENCIES_FALLBACK]);
     });
   });
+
+  describe('fetchSupportedNetworks', () => {
+    afterEach(() => {
+      resetSupportedNetworksCache();
+    });
+
+    it('fetches supported networks from the API and returns them', async () => {
+      const mockResponse = {
+        fullSupport: ['eip155:1', 'eip155:137'],
+        partialSupport: {
+          spotPricesV2: ['eip155:1', 'eip155:137', 'eip155:56'],
+          spotPricesV3: ['eip155:1', 'eip155:137', 'eip155:42161'],
+        },
+      };
+      nock('https://price.api.cx.metamask.io')
+        .get('/v2/supportedNetworks')
+        .reply(200, mockResponse);
+
+      const result = await fetchSupportedNetworks();
+
+      expect(result).toStrictEqual(mockResponse);
+    });
+
+    it('returns the fallback list when the API returns an invalid response', async () => {
+      nock('https://price.api.cx.metamask.io')
+        .get('/v2/supportedNetworks')
+        .reply(200, { invalid: 'response' });
+
+      const result = await fetchSupportedNetworks();
+
+      expect(result.fullSupport).toBeDefined();
+      expect(result.partialSupport).toBeDefined();
+      expect(result.partialSupport.spotPricesV3).toBeDefined();
+    });
+
+    it('returns the fallback list when the API request fails', async () => {
+      nock('https://price.api.cx.metamask.io')
+        .get('/v2/supportedNetworks')
+        .replyWithError('Network error');
+
+      const result = await fetchSupportedNetworks();
+
+      expect(result.fullSupport).toBeDefined();
+      expect(result.partialSupport).toBeDefined();
+      expect(result.partialSupport.spotPricesV3).toBeDefined();
+    });
+
+    it('updates getSupportedNetworks after a successful fetch', async () => {
+      const mockResponse = {
+        fullSupport: ['eip155:1'],
+        partialSupport: {
+          spotPricesV2: ['eip155:1', 'eip155:56'],
+          spotPricesV3: ['eip155:1', 'eip155:42161'],
+        },
+      };
+      nock('https://price.api.cx.metamask.io')
+        .get('/v2/supportedNetworks')
+        .reply(200, mockResponse);
+
+      await fetchSupportedNetworks();
+      const result = getSupportedNetworks();
+
+      expect(result).toStrictEqual(mockResponse);
+    });
+  });
+
+  describe('getSupportedNetworks', () => {
+    beforeEach(() => {
+      resetSupportedNetworksCache();
+    });
+
+    it('returns the fallback list when no networks have been fetched', () => {
+      const result = getSupportedNetworks();
+
+      expect(result.fullSupport).toBeDefined();
+      expect(result.partialSupport).toBeDefined();
+      expect(result.partialSupport.spotPricesV3).toBeDefined();
+      expect(Array.isArray(result.fullSupport)).toBe(true);
+      expect(Array.isArray(result.partialSupport.spotPricesV3)).toBe(true);
+    });
+  });
+
+  describe('updateSupportedNetworks', () => {
+    afterEach(() => {
+      resetSupportedNetworksCache();
+    });
+
+    it('fetches and returns supported networks via the service method', async () => {
+      const mockResponse = {
+        fullSupport: ['eip155:1', 'eip155:10'],
+        partialSupport: {
+          spotPricesV2: ['eip155:1'],
+          spotPricesV3: ['eip155:1', 'eip155:10'],
+        },
+      };
+      nock('https://price.api.cx.metamask.io')
+        .get('/v2/supportedNetworks')
+        .reply(200, mockResponse);
+
+      const service = new CodefiTokenPricesServiceV2();
+      const result = await service.updateSupportedNetworks();
+
+      expect(result).toStrictEqual(mockResponse);
+    });
+
+    it('returns the fallback list when the API fails', async () => {
+      nock('https://price.api.cx.metamask.io')
+        .get('/v2/supportedNetworks')
+        .replyWithError('Network error');
+
+      const service = new CodefiTokenPricesServiceV2();
+      const result = await service.updateSupportedNetworks();
+
+      expect(result.fullSupport).toBeDefined();
+      expect(result.partialSupport).toBeDefined();
+    });
+  });
+
+  describe('setNativeAssetIdentifiers', () => {
+    afterEach(() => {
+      resetSupportedNetworksCache();
+    });
+
+    it('sets native asset identifiers and uses them in fetchTokenPrices', async () => {
+      // Mock supportedNetworks to include our test chain
+      const mockNetworksResponse = {
+        fullSupport: ['eip155:1'],
+        partialSupport: {
+          spotPricesV2: [],
+          spotPricesV3: ['eip155:1'],
+        },
+      };
+      nock('https://price.api.cx.metamask.io')
+        .get('/v2/supportedNetworks')
+        .reply(200, mockNetworksResponse)
+        .persist();
+
+      // Pre-populate the cache
+      await fetchSupportedNetworks();
+
+      const customNativeAssetId = 'eip155:1/slip44:60';
+      const nativeAssetIdentifiers = {
+        'eip155:1': customNativeAssetId,
+      };
+
+      // Mock the spot-prices response
+      nock('https://price.api.cx.metamask.io')
+        .get('/v3/spot-prices')
+        .query(true)
+        .reply(200, {
+          [customNativeAssetId]: {
+            price: 2000,
+            currency: 'USD',
+            pricePercentChange1d: 1,
+            priceChange1d: 1,
+            marketCap: 1000000,
+            allTimeHigh: 5000,
+            allTimeLow: 100,
+            totalVolume: 50000,
+            high1d: 2100,
+            low1d: 1900,
+            circulatingSupply: 1000000,
+            dilutedMarketCap: 2000000,
+            marketCapPercentChange1d: 0.5,
+            pricePercentChange1h: 0.1,
+            pricePercentChange7d: 5,
+            pricePercentChange14d: 10,
+            pricePercentChange30d: 15,
+            pricePercentChange200d: 50,
+            pricePercentChange1y: 100,
+          },
+        });
+
+      const service = new CodefiTokenPricesServiceV2();
+      service.setNativeAssetIdentifiers(
+        nativeAssetIdentifiers as Record<
+          `${string}:${string}`,
+          `${string}:${string}/${string}:${string}`
+        >,
+      );
+
+      const result = await service.fetchTokenPrices({
+        assets: [{ chainId: '0x1', tokenAddress: ZERO_ADDRESS }],
+        currency: 'USD',
+      });
+
+      expect(result).toHaveLength(1);
+      expect(result[0].price).toBe(2000);
+    });
+  });
+
+  describe('validateChainIdSupported with dynamic networks', () => {
+    afterEach(() => {
+      resetSupportedNetworksCache();
+    });
+
+    it('returns true for chains in the dynamic supported networks list', async () => {
+      const mockResponse = {
+        fullSupport: ['eip155:999999'],
+        partialSupport: {
+          spotPricesV2: [],
+          spotPricesV3: ['eip155:999999'],
+        },
+      };
+      nock('https://price.api.cx.metamask.io')
+        .get('/v2/supportedNetworks')
+        .reply(200, mockResponse);
+
+      await fetchSupportedNetworks();
+
+      const service = new CodefiTokenPricesServiceV2();
+      // 0xf423f = 999999 in hex
+      expect(service.validateChainIdSupported('0xf423f')).toBe(true);
+    });
+
+    it('returns true for chains in the hardcoded fallback list', () => {
+      resetSupportedNetworksCache();
+
+      const service = new CodefiTokenPricesServiceV2();
+      // 0x1 (Ethereum mainnet) should always be in the hardcoded list
+      expect(service.validateChainIdSupported('0x1')).toBe(true);
+    });
+
+    it('returns false for unsupported chains', () => {
+      resetSupportedNetworksCache();
+
+      const service = new CodefiTokenPricesServiceV2();
+      // Some random chain ID that's not supported
+      expect(service.validateChainIdSupported('0xdeadbeef')).toBe(false);
+    });
+  });
 });
 
 /**
diff --git a/packages/assets-controllers/src/token-prices-service/codefi-v2.ts b/packages/assets-controllers/src/token-prices-service/codefi-v2.ts
index 4a5092d0865..0d026278b25 100644
--- a/packages/assets-controllers/src/token-prices-service/codefi-v2.ts
+++ b/packages/assets-controllers/src/token-prices-service/codefi-v2.ts
@@ -11,6 +11,7 @@ import type { CaipAssetType, Hex } from '@metamask/utils';
 import {
   hexToNumber,
   KnownCaipNamespace,
+  numberToHex,
   toCaipChainId,
 } from '@metamask/utils';
 
@@ -20,6 +21,7 @@ import type {
   EvmAssetWithId,
   EvmAssetWithMarketData,
   ExchangeRatesByCurrency,
+  NativeAssetIdentifiersMap,
 } from './abstract-token-prices-service';
 import type { MarketDataDetails } from '../TokenRatesController';
 
@@ -343,20 +345,132 @@ export const SUPPORTED_CHAIN_IDS = Object.keys(
  */
 type SupportedChainId = (typeof SUPPORTED_CHAIN_IDS)[number];
 
+const BASE_URL_V1 = 'https://price.api.cx.metamask.io/v1';
+
+const BASE_URL_V2 = 'https://price.api.cx.metamask.io/v2';
+
+const BASE_URL_V3 = 'https://price.api.cx.metamask.io/v3';
+
 /**
- * The list of chain IDs that are supported by V3 of the Codefi Price API.
- * Only includes chain IDs from SPOT_PRICES_SUPPORT_INFO that have a non-null CAIP-19 value.
+ * Response type for the /v2/supportedNetworks endpoint.
  */
-const SUPPORTED_CHAIN_IDS_V3 = Object.keys(SPOT_PRICES_SUPPORT_INFO).filter(
-  (chainId) =>
-    SPOT_PRICES_SUPPORT_INFO[
-      chainId as keyof typeof SPOT_PRICES_SUPPORT_INFO
-    ] !== null,
-);
+type SupportedNetworksResponse = {
+  fullSupport: string[];
+  partialSupport: {
+    spotPricesV2: string[];
+    spotPricesV3: string[];
+  };
+};
 
-const BASE_URL_V1 = 'https://price.api.cx.metamask.io/v1';
+/**
+ * In-memory store for the last successfully fetched supported networks.
+ */
+let lastFetchedSupportedNetworks: SupportedNetworksResponse | null = null;
 
-const BASE_URL_V3 = 'https://price.api.cx.metamask.io/v3';
+/**
+ * Converts a CAIP-2 chain ID (e.g., 'eip155:1') to a hex chain ID (e.g., '0x1').
+ *
+ * @param caipChainId - The CAIP-2 chain ID string.
+ * @returns The hex chain ID or null if not an EIP-155 chain.
+ */
+function caipChainIdToHex(caipChainId: string): Hex | null {
+  const match = caipChainId.match(/^eip155:(\d+)$/u);
+  if (!match) {
+    return null;
+  }
+  return numberToHex(parseInt(match[1], 10));
+}
+
+/**
+ * Fetches the list of supported networks from the API.
+ * Falls back to the hardcoded list if the fetch fails.
+ *
+ * @returns The supported networks response.
+ */
+export async function fetchSupportedNetworks(): Promise<SupportedNetworksResponse> {
+  try {
+    const url = `${BASE_URL_V2}/supportedNetworks`;
+    const response = await handleFetch(url, {
+      headers: { 'Cache-Control': 'no-cache' },
+    });
+
+    if (
+      response &&
+      typeof response === 'object' &&
+      'fullSupport' in response &&
+      'partialSupport' in response
+    ) {
+      lastFetchedSupportedNetworks = response as SupportedNetworksResponse;
+      return lastFetchedSupportedNetworks;
+    }
+
+    // Invalid response format, fall back to hardcoded list
+    return getSupportedNetworksFallback();
+  } catch {
+    // On any error, fall back to the hardcoded list
+    return getSupportedNetworksFallback();
+  }
+}
+
+/**
+ * Synchronously gets the list of supported networks.
+ * Returns the last fetched value if available, otherwise returns the fallback list.
+ *
+ * @returns The supported networks response.
+ */
+export function getSupportedNetworks(): SupportedNetworksResponse {
+  if (lastFetchedSupportedNetworks !== null) {
+    return lastFetchedSupportedNetworks;
+  }
+  return getSupportedNetworksFallback();
+}
+
+/**
+ * Generates a fallback supported networks response from the hardcoded SPOT_PRICES_SUPPORT_INFO.
+ *
+ * @returns A SupportedNetworksResponse derived from hardcoded data.
+ */
+function getSupportedNetworksFallback(): SupportedNetworksResponse {
+  const caipChainIds = Object.keys(SPOT_PRICES_SUPPORT_INFO).map((hexChainId) =>
+    toCaipChainId(
+      KnownCaipNamespace.Eip155,
+      hexToNumber(hexChainId as Hex).toString(),
+    ),
+  );
+
+  return {
+    fullSupport: caipChainIds.slice(0, 11), // First 11 chains as "full support"
+    partialSupport: {
+      spotPricesV2: caipChainIds,
+      spotPricesV3: caipChainIds,
+    },
+  };
+}
+
+/**
+ * Resets the supported networks cache.
+ * This is primarily intended for testing purposes.
+ */
+export function resetSupportedNetworksCache(): void {
+  lastFetchedSupportedNetworks = null;
+}
+
+/**
+ * Gets the list of supported chain IDs for spot prices v3 as hex values.
+ *
+ * @returns Array of hex chain IDs supported by spot prices v3.
+ */
+function getSupportedChainIdsV3AsHex(): Hex[] {
+  const supportedNetworks = getSupportedNetworks();
+  const allV3Chains = [
+    ...supportedNetworks.fullSupport,
+    ...supportedNetworks.partialSupport.spotPricesV3,
+  ];
+
+  return allV3Chains
+    .map(caipChainIdToHex)
+    .filter((hexChainId): hexChainId is Hex => hexChainId !== null);
+}
 
 /**
  * In-memory store for the last successfully fetched supported currencies.
@@ -422,6 +536,12 @@ export class CodefiTokenPricesServiceV2
 {
   readonly #policy: ServicePolicy;
 
+  /**
+   * Map of CAIP-2 chain IDs to their native asset identifiers.
+   * Updated via setNativeAssetIdentifiers().
+   */
+  #nativeAssetIdentifiers: NativeAssetIdentifiersMap = {};
+
   /**
    * Construct a Codefi Token Price Service.
    *
@@ -526,6 +646,28 @@ export class CodefiTokenPricesServiceV2
     return this.#policy.onDegraded(...args);
   }
 
+  /**
+   * Sets the native asset identifiers map for resolving native token CAIP-19 IDs.
+   * This should be called with data from NetworkEnablementController.state.nativeAssetIdentifiers.
+   *
+   * @param nativeAssetIdentifiers - Map of CAIP-2 chain IDs to native asset identifiers.
+   */
+  setNativeAssetIdentifiers(
+    nativeAssetIdentifiers: NativeAssetIdentifiersMap,
+  ): void {
+    this.#nativeAssetIdentifiers = nativeAssetIdentifiers;
+  }
+
+  /**
+   * Updates the supported networks cache by fetching from the API.
+   * This should be called periodically to keep the supported networks list fresh.
+   *
+   * @returns The updated supported networks response.
+   */
+  async updateSupportedNetworks(): Promise<SupportedNetworksResponse> {
+    return fetchSupportedNetworks();
+  }
+
   /**
    * Retrieves prices in the given currency for the tokens identified by the
    * given addresses which are expected to live on the given chain.
@@ -542,9 +684,18 @@ export class CodefiTokenPricesServiceV2
     assets: EvmAssetAddressWithChain<SupportedChainId>[];
     currency: SupportedCurrency;
   }): Promise<EvmAssetWithMarketData<SupportedChainId, SupportedCurrency>[]> {
+    // Refresh supported networks in background (non-blocking)
+    // This ensures the list stays fresh during normal polling
+    // Note: fetchSupportedNetworks handles errors internally and always resolves
+    // eslint-disable-next-line @typescript-eslint/no-floating-promises
+    fetchSupportedNetworks();
+
+    // Get dynamically fetched supported chain IDs for V3
+    const supportedChainIdsV3 = getSupportedChainIdsV3AsHex();
+
     const assetsWithIds: EvmAssetWithId<SupportedChainId>[] = assets
       // Filter out assets that are not supported by V3 of the Price API.
-      .filter((asset) => SUPPORTED_CHAIN_IDS_V3.includes(asset.chainId))
+      .filter((asset) => supportedChainIdsV3.includes(asset.chainId))
       .map((asset) => {
         const caipChainId = toCaipChainId(
           KnownCaipNamespace.Eip155,
@@ -552,16 +703,34 @@ export class CodefiTokenPricesServiceV2
         );
 
         const nativeAddress = getNativeTokenAddress(asset.chainId);
+        const isNativeToken =
+          nativeAddress.toLowerCase() === asset.tokenAddress.toLowerCase();
+
+        let assetId: string | undefined;
+        if (isNativeToken) {
+          // For native tokens, use nativeAssetIdentifiers from NetworkEnablementController,
+          // falling back to hardcoded SPOT_PRICES_SUPPORT_INFO
+          assetId =
+            this.#nativeAssetIdentifiers[caipChainId] ??
+            SPOT_PRICES_SUPPORT_INFO[asset.chainId];
+        } else {
+          // For ERC20 tokens, construct the CAIP-19 ID dynamically
+          assetId = `${caipChainId}/erc20:${asset.tokenAddress.toLowerCase()}`;
+        }
+
+        if (!assetId) {
+          return undefined;
+        }
 
         return {
           ...asset,
-          assetId: (nativeAddress.toLowerCase() ===
-          asset.tokenAddress.toLowerCase()
-            ? SPOT_PRICES_SUPPORT_INFO[asset.chainId]
-            : `${caipChainId}/erc20:${asset.tokenAddress.toLowerCase()}`) as CaipAssetType,
+          assetId: assetId as CaipAssetType,
         };
       })
-      .filter((asset) => asset.assetId);
+      .filter(
+        (asset): asset is EvmAssetWithId<SupportedChainId> =>
+          asset !== undefined,
+      );
 
     if (assetsWithIds.length === 0) {
       return [];
@@ -717,8 +886,15 @@ export class CodefiTokenPricesServiceV2
    * @returns True if the API supports the chain ID, false otherwise.
    */
   validateChainIdSupported(chainId: unknown): chainId is SupportedChainId {
-    const supportedChainIds: readonly string[] = SUPPORTED_CHAIN_IDS;
-    return typeof chainId === 'string' && supportedChainIds.includes(chainId);
+    // Use dynamically fetched supported networks
+    const supportedChainIds = getSupportedChainIdsV3AsHex();
+    // Also include the hardcoded fallback list for backwards compatibility
+    const allSupportedChainIds: readonly string[] = [
+      ...new Set([...supportedChainIds, ...SUPPORTED_CHAIN_IDS]),
+    ];
+    return (
+      typeof chainId === 'string' && allSupportedChainIds.includes(chainId)
+    );
   }
 
   /**
diff --git a/packages/assets-controllers/src/token-prices-service/index.test.ts b/packages/assets-controllers/src/token-prices-service/index.test.ts
index a59be2ba4de..13ffb135df6 100644
--- a/packages/assets-controllers/src/token-prices-service/index.test.ts
+++ b/packages/assets-controllers/src/token-prices-service/index.test.ts
@@ -7,6 +7,9 @@ describe('token-prices-service', () => {
         "CodefiTokenPricesServiceV2",
         "SUPPORTED_CHAIN_IDS",
         "getNativeTokenAddress",
+        "fetchSupportedNetworks",
+        "getSupportedNetworks",
+        "resetSupportedNetworksCache",
       ]
     `);
   });
diff --git a/packages/assets-controllers/src/token-prices-service/index.ts b/packages/assets-controllers/src/token-prices-service/index.ts
index 509fc680055..cb788010df2 100644
--- a/packages/assets-controllers/src/token-prices-service/index.ts
+++ b/packages/assets-controllers/src/token-prices-service/index.ts
@@ -1,6 +1,12 @@
-export type { AbstractTokenPricesService } from './abstract-token-prices-service';
+export type {
+  AbstractTokenPricesService,
+  NativeAssetIdentifiersMap,
+} from './abstract-token-prices-service';
 export {
   CodefiTokenPricesServiceV2,
   SUPPORTED_CHAIN_IDS,
   getNativeTokenAddress,
+  fetchSupportedNetworks,
+  getSupportedNetworks,
+  resetSupportedNetworksCache,
 } from './codefi-v2';
diff --git a/packages/assets-controllers/tsconfig.build.json b/packages/assets-controllers/tsconfig.build.json
index 5ef0e52c3b8..cd6fefbce28 100644
--- a/packages/assets-controllers/tsconfig.build.json
+++ b/packages/assets-controllers/tsconfig.build.json
@@ -14,6 +14,7 @@
     { "path": "../controller-utils/tsconfig.build.json" },
     { "path": "../keyring-controller/tsconfig.build.json" },
     { "path": "../network-controller/tsconfig.build.json" },
+    { "path": "../network-enablement-controller/tsconfig.build.json" },
     { "path": "../messenger/tsconfig.build.json" },
     { "path": "../preferences-controller/tsconfig.build.json" },
     { "path": "../polling-controller/tsconfig.build.json" },
diff --git a/packages/assets-controllers/tsconfig.json b/packages/assets-controllers/tsconfig.json
index a537b98ca39..88b08f3986a 100644
--- a/packages/assets-controllers/tsconfig.json
+++ b/packages/assets-controllers/tsconfig.json
@@ -13,6 +13,7 @@
     { "path": "../controller-utils" },
     { "path": "../keyring-controller" },
     { "path": "../network-controller" },
+    { "path": "../network-enablement-controller" },
     { "path": "../messenger" },
     { "path": "../preferences-controller" },
     { "path": "../phishing-controller" },
diff --git a/yarn.lock b/yarn.lock
index d05973886ae..3a8cba0ba74 100644
--- a/yarn.lock
+++ b/yarn.lock
@@ -2704,6 +2704,7 @@ __metadata:
     "@metamask/metamask-eth-abis": "npm:^3.1.1"
     "@metamask/multichain-account-service": "npm:^5.1.0"
     "@metamask/network-controller": "npm:^29.0.0"
+    "@metamask/network-enablement-controller": "npm:^4.1.0"
     "@metamask/permission-controller": "npm:^12.2.0"
     "@metamask/phishing-controller": "npm:^16.1.0"
     "@metamask/polling-controller": "npm:^16.0.2"