diff --git a/packages/assets-controllers/CHANGELOG.md b/packages/assets-controllers/CHANGELOG.md
index 4b4d811666..950f291d68 100644
--- a/packages/assets-controllers/CHANGELOG.md
+++ b/packages/assets-controllers/CHANGELOG.md
@@ -14,6 +14,8 @@ and this project adheres to [Semantic Versioning](https://semver.org/spec/v2.0.0
   - This should be functionally equivalent, but is being noted anyway.
 - NftDetectionController now makes use of `selectedNetworkClientId` when responding to changes in NetworkController state to capture the currently selected chain rather than `providerConfig` ([#4307](https://github.com/MetaMask/core/pull/4307))
   - This should be functionally equivalent, but is being noted anyway.
+- TokenRatesController now makes use of `selectedNetworkClientId` when responding to changes in NetworkController state to capture the currently selected chain rather than `providerConfig` ([#4317](https://github.com/MetaMask/core/pull/4317))
+  - This should be functionally equivalent, but is being noted anyway.
 
 ## [29.0.0]
 
diff --git a/packages/assets-controllers/src/TokenRatesController.test.ts b/packages/assets-controllers/src/TokenRatesController.test.ts
index a82a195ff7..d5d0ae8701 100644
--- a/packages/assets-controllers/src/TokenRatesController.test.ts
+++ b/packages/assets-controllers/src/TokenRatesController.test.ts
@@ -1,16 +1,28 @@
 import {
+  ChainId,
+  InfuraNetworkType,
   NetworksTicker,
   toChecksumHexAddress,
   toHex,
 } from '@metamask/controller-utils';
-import type { NetworkState } from '@metamask/network-controller';
+import type {
+  NetworkClientConfiguration,
+  NetworkClientId,
+  NetworkState,
+} from '@metamask/network-controller';
+import { defaultState as defaultNetworkState } from '@metamask/network-controller';
 import type { PreferencesState } from '@metamask/preferences-controller';
 import type { Hex } from '@metamask/utils';
 import { add0x } from '@metamask/utils';
+import assert from 'assert';
 import nock from 'nock';
 import { useFakeTimers } from 'sinon';
 
 import { advanceTime, flushPromises } from '../../../tests/helpers';
+import {
+  buildCustomNetworkClientConfiguration,
+  buildMockGetNetworkClientById,
+} from '../../network-controller/tests/helpers';
 import { TOKEN_PRICES_BATCH_SIZE } from './assetsUtil';
 import type {
   AbstractTokenPricesService,
@@ -738,9 +750,13 @@ describe('TokenRatesController', () => {
 
     describe('when polling is active', () => {
       it('should update exchange rates when ticker changes', async () => {
-        // TODO: Replace `any` with type
-        // eslint-disable-next-line @typescript-eslint/no-explicit-any
-        let networkStateChangeListener: (state: any) => Promise<void>;
+        const getNetworkClientById = buildMockGetNetworkClientById({
+          'AAAA-BBBB-CCCC-DDDD': buildCustomNetworkClientConfiguration({
+            chainId: toHex(1337),
+            ticker: 'NEW',
+          }),
+        });
+        let networkStateChangeListener: (state: NetworkState) => Promise<void>;
         const onNetworkStateChange = jest
           .fn()
           .mockImplementation((listener) => {
@@ -748,7 +764,7 @@ describe('TokenRatesController', () => {
           });
         const controller = new TokenRatesController({
           interval: 100,
-          getNetworkClientById: jest.fn(),
+          getNetworkClientById,
           chainId: toHex(1337),
           ticker: 'TEST',
           selectedAddress: defaultSelectedAddress,
@@ -764,16 +780,21 @@ describe('TokenRatesController', () => {
 
         // eslint-disable-next-line @typescript-eslint/no-non-null-assertion
         await networkStateChangeListener!({
-          providerConfig: { chainId: toHex(1337), ticker: 'NEW' },
+          ...defaultNetworkState,
+          selectedNetworkClientId: 'AAAA-BBBB-CCCC-DDDD',
         });
 
         expect(updateExchangeRatesSpy).toHaveBeenCalledTimes(1);
       });
 
       it('should update exchange rates when chain ID changes', async () => {
-        // TODO: Replace `any` with type
-        // eslint-disable-next-line @typescript-eslint/no-explicit-any
-        let networkStateChangeListener: (state: any) => Promise<void>;
+        const getNetworkClientById = buildMockGetNetworkClientById({
+          'AAAA-BBBB-CCCC-DDDD': buildCustomNetworkClientConfiguration({
+            chainId: toHex(1338),
+            ticker: 'TEST',
+          }),
+        });
+        let networkStateChangeListener: (state: NetworkState) => Promise<void>;
         const onNetworkStateChange = jest
           .fn()
           .mockImplementation((listener) => {
@@ -781,7 +802,7 @@ describe('TokenRatesController', () => {
           });
         const controller = new TokenRatesController({
           interval: 100,
-          getNetworkClientById: jest.fn(),
+          getNetworkClientById,
           chainId: toHex(1337),
           ticker: 'TEST',
           selectedAddress: defaultSelectedAddress,
@@ -797,16 +818,21 @@ describe('TokenRatesController', () => {
 
         // eslint-disable-next-line @typescript-eslint/no-non-null-assertion
         await networkStateChangeListener!({
-          providerConfig: { chainId: toHex(1338), ticker: 'TEST' },
+          ...defaultNetworkState,
+          selectedNetworkClientId: 'AAAA-BBBB-CCCC-DDDD',
         });
 
         expect(updateExchangeRatesSpy).toHaveBeenCalledTimes(1);
       });
 
       it('should clear contractExchangeRates state when ticker changes', async () => {
-        // TODO: Replace `any` with type
-        // eslint-disable-next-line @typescript-eslint/no-explicit-any
-        let networkStateChangeListener: (state: any) => Promise<void>;
+        const getNetworkClientById = buildMockGetNetworkClientById({
+          'AAAA-BBBB-CCCC-DDDD': buildCustomNetworkClientConfiguration({
+            chainId: toHex(1337),
+            ticker: 'NEW',
+          }),
+        });
+        let networkStateChangeListener: (state: NetworkState) => Promise<void>;
         const onNetworkStateChange = jest
           .fn()
           .mockImplementation((listener) => {
@@ -814,7 +840,7 @@ describe('TokenRatesController', () => {
           });
         const controller = new TokenRatesController({
           interval: 100,
-          getNetworkClientById: jest.fn(),
+          getNetworkClientById,
           chainId: toHex(1337),
           ticker: 'TEST',
           selectedAddress: defaultSelectedAddress,
@@ -828,16 +854,21 @@ describe('TokenRatesController', () => {
 
         // eslint-disable-next-line @typescript-eslint/no-non-null-assertion
         await networkStateChangeListener!({
-          providerConfig: { chainId: toHex(1337), ticker: 'NEW' },
+          ...defaultNetworkState,
+          selectedNetworkClientId: 'AAAA-BBBB-CCCC-DDDD',
         });
 
         expect(controller.state.contractExchangeRates).toStrictEqual({});
       });
 
       it('should clear contractExchangeRates state when chain ID changes', async () => {
-        // TODO: Replace `any` with type
-        // eslint-disable-next-line @typescript-eslint/no-explicit-any
-        let networkStateChangeListener: (state: any) => Promise<void>;
+        const getNetworkClientById = buildMockGetNetworkClientById({
+          'AAAA-BBBB-CCCC-DDDD': buildCustomNetworkClientConfiguration({
+            chainId: toHex(1338),
+            ticker: 'TEST',
+          }),
+        });
+        let networkStateChangeListener: (state: NetworkState) => Promise<void>;
         const onNetworkStateChange = jest
           .fn()
           .mockImplementation((listener) => {
@@ -845,7 +876,7 @@ describe('TokenRatesController', () => {
           });
         const controller = new TokenRatesController({
           interval: 100,
-          getNetworkClientById: jest.fn(),
+          getNetworkClientById,
           chainId: toHex(1337),
           ticker: 'TEST',
           selectedAddress: defaultSelectedAddress,
@@ -859,16 +890,21 @@ describe('TokenRatesController', () => {
 
         // eslint-disable-next-line @typescript-eslint/no-non-null-assertion
         await networkStateChangeListener!({
-          providerConfig: { chainId: toHex(1338), ticker: 'TEST' },
+          ...defaultNetworkState,
+          selectedNetworkClientId: 'AAAA-BBBB-CCCC-DDDD',
         });
 
         expect(controller.state.contractExchangeRates).toStrictEqual({});
       });
 
       it('should not update exchange rates when network state changes without a ticker/chain id change', async () => {
-        // TODO: Replace `any` with type
-        // eslint-disable-next-line @typescript-eslint/no-explicit-any
-        let networkStateChangeListener: (state: any) => Promise<void>;
+        const getNetworkClientById = buildMockGetNetworkClientById({
+          'AAAA-BBBB-CCCC-DDDD': buildCustomNetworkClientConfiguration({
+            chainId: toHex(1337),
+            ticker: 'TEST',
+          }),
+        });
+        let networkStateChangeListener: (state: NetworkState) => Promise<void>;
         const onNetworkStateChange = jest
           .fn()
           .mockImplementation((listener) => {
@@ -876,7 +912,7 @@ describe('TokenRatesController', () => {
           });
         const controller = new TokenRatesController({
           interval: 100,
-          getNetworkClientById: jest.fn(),
+          getNetworkClientById,
           chainId: toHex(1337),
           ticker: 'TEST',
           selectedAddress: defaultSelectedAddress,
@@ -892,7 +928,8 @@ describe('TokenRatesController', () => {
 
         // eslint-disable-next-line @typescript-eslint/no-non-null-assertion
         await networkStateChangeListener!({
-          providerConfig: { chainId: toHex(1337), ticker: 'TEST' },
+          ...defaultNetworkState,
+          selectedNetworkClientId: 'AAAA-BBBB-CCCC-DDDD',
         });
 
         expect(updateExchangeRatesSpy).not.toHaveBeenCalled();
@@ -901,9 +938,13 @@ describe('TokenRatesController', () => {
 
     describe('when polling is inactive', () => {
       it('should not update exchange rates when ticker changes', async () => {
-        // TODO: Replace `any` with type
-        // eslint-disable-next-line @typescript-eslint/no-explicit-any
-        let networkStateChangeListener: (state: any) => Promise<void>;
+        const getNetworkClientById = buildMockGetNetworkClientById({
+          'AAAA-BBBB-CCCC-DDDD': buildCustomNetworkClientConfiguration({
+            chainId: toHex(1337),
+            ticker: 'NEW',
+          }),
+        });
+        let networkStateChangeListener: (state: NetworkState) => Promise<void>;
         const onNetworkStateChange = jest
           .fn()
           .mockImplementation((listener) => {
@@ -911,7 +952,7 @@ describe('TokenRatesController', () => {
           });
         const controller = new TokenRatesController({
           interval: 100,
-          getNetworkClientById: jest.fn(),
+          getNetworkClientById,
           chainId: toHex(1337),
           ticker: 'TEST',
           selectedAddress: defaultSelectedAddress,
@@ -926,16 +967,21 @@ describe('TokenRatesController', () => {
 
         // eslint-disable-next-line @typescript-eslint/no-non-null-assertion
         await networkStateChangeListener!({
-          providerConfig: { chainId: toHex(1337), ticker: 'NEW' },
+          ...defaultNetworkState,
+          selectedNetworkClientId: 'AAAA-BBBB-CCCC-DDDD',
         });
 
         expect(updateExchangeRatesSpy).not.toHaveBeenCalled();
       });
 
       it('should not update exchange rates when chain ID changes', async () => {
-        // TODO: Replace `any` with type
-        // eslint-disable-next-line @typescript-eslint/no-explicit-any
-        let networkStateChangeListener: (state: any) => Promise<void>;
+        const getNetworkClientById = buildMockGetNetworkClientById({
+          'AAAA-BBBB-CCCC-DDDD': buildCustomNetworkClientConfiguration({
+            chainId: toHex(1338),
+            ticker: 'TEST',
+          }),
+        });
+        let networkStateChangeListener: (state: NetworkState) => Promise<void>;
         const onNetworkStateChange = jest
           .fn()
           .mockImplementation((listener) => {
@@ -943,7 +989,7 @@ describe('TokenRatesController', () => {
           });
         const controller = new TokenRatesController({
           interval: 100,
-          getNetworkClientById: jest.fn(),
+          getNetworkClientById,
           chainId: toHex(1337),
           ticker: 'TEST',
           selectedAddress: defaultSelectedAddress,
@@ -958,16 +1004,21 @@ describe('TokenRatesController', () => {
 
         // eslint-disable-next-line @typescript-eslint/no-non-null-assertion
         await networkStateChangeListener!({
-          providerConfig: { chainId: toHex(1338), ticker: 'TEST' },
+          ...defaultNetworkState,
+          selectedNetworkClientId: 'AAAA-BBBB-CCCC-DDDD',
         });
 
         expect(updateExchangeRatesSpy).not.toHaveBeenCalled();
       });
 
       it('should clear contractExchangeRates state when ticker changes', async () => {
-        // TODO: Replace `any` with type
-        // eslint-disable-next-line @typescript-eslint/no-explicit-any
-        let networkStateChangeListener: (state: any) => Promise<void>;
+        const getNetworkClientById = buildMockGetNetworkClientById({
+          'AAAA-BBBB-CCCC-DDDD': buildCustomNetworkClientConfiguration({
+            chainId: toHex(1337),
+            ticker: 'NEW',
+          }),
+        });
+        let networkStateChangeListener: (state: NetworkState) => Promise<void>;
         const onNetworkStateChange = jest
           .fn()
           .mockImplementation((listener) => {
@@ -975,7 +1026,7 @@ describe('TokenRatesController', () => {
           });
         const controller = new TokenRatesController({
           interval: 100,
-          getNetworkClientById: jest.fn(),
+          getNetworkClientById,
           chainId: toHex(1337),
           ticker: 'TEST',
           selectedAddress: defaultSelectedAddress,
@@ -988,16 +1039,21 @@ describe('TokenRatesController', () => {
 
         // eslint-disable-next-line @typescript-eslint/no-non-null-assertion
         await networkStateChangeListener!({
-          providerConfig: { chainId: toHex(1337), ticker: 'NEW' },
+          ...defaultNetworkState,
+          selectedNetworkClientId: 'AAAA-BBBB-CCCC-DDDD',
         });
 
         expect(controller.state.contractExchangeRates).toStrictEqual({});
       });
 
       it('should clear contractExchangeRates state when chain ID changes', async () => {
-        // TODO: Replace `any` with type
-        // eslint-disable-next-line @typescript-eslint/no-explicit-any
-        let networkStateChangeListener: (state: any) => Promise<void>;
+        const getNetworkClientById = buildMockGetNetworkClientById({
+          'AAAA-BBBB-CCCC-DDDD': buildCustomNetworkClientConfiguration({
+            chainId: toHex(1338),
+            ticker: 'TEST',
+          }),
+        });
+        let networkStateChangeListener: (state: NetworkState) => Promise<void>;
         const onNetworkStateChange = jest
           .fn()
           .mockImplementation((listener) => {
@@ -1005,7 +1061,7 @@ describe('TokenRatesController', () => {
           });
         const controller = new TokenRatesController({
           interval: 100,
-          getNetworkClientById: jest.fn(),
+          getNetworkClientById,
           chainId: toHex(1337),
           ticker: 'TEST',
           selectedAddress: defaultSelectedAddress,
@@ -1018,7 +1074,8 @@ describe('TokenRatesController', () => {
 
         // eslint-disable-next-line @typescript-eslint/no-non-null-assertion
         await networkStateChangeListener!({
-          providerConfig: { chainId: toHex(1338), ticker: 'TEST' },
+          ...defaultNetworkState,
+          selectedNetworkClientId: 'AAAA-BBBB-CCCC-DDDD',
         });
 
         expect(controller.state.contractExchangeRates).toStrictEqual({});
@@ -1604,7 +1661,7 @@ describe('TokenRatesController', () => {
 
           await callUpdateExchangeRatesMethod({
             allTokens: {
-              [toHex(1)]: {
+              [ChainId.mainnet]: {
                 [controller.config.selectedAddress]: [
                   {
                     address: tokenAddress,
@@ -1615,11 +1672,12 @@ describe('TokenRatesController', () => {
                 ],
               },
             },
-            chainId: toHex(1),
+            chainId: ChainId.mainnet,
             controller,
             controllerEvents,
             method,
             nativeCurrency: 'ETH',
+            selectedNetworkClientId: InfuraNetworkType.mainnet,
           });
 
           expect(controller.state.contractExchangeRates).toStrictEqual({});
@@ -1638,7 +1696,7 @@ describe('TokenRatesController', () => {
         await callUpdateExchangeRatesMethod({
           allTokens: {
             // These tokens are for the right chain but wrong account
-            [toHex(1)]: {
+            [ChainId.mainnet]: {
               [differentAccount]: [
                 {
                   address: tokenAddress,
@@ -1660,11 +1718,12 @@ describe('TokenRatesController', () => {
               ],
             },
           },
-          chainId: toHex(1),
+          chainId: ChainId.mainnet,
           controller,
           controllerEvents,
           method,
           nativeCurrency: 'ETH',
+          selectedNetworkClientId: InfuraNetworkType.mainnet,
         });
 
         expect(controller.state.contractExchangeRates).toStrictEqual({});
@@ -1689,7 +1748,7 @@ describe('TokenRatesController', () => {
             async () =>
               await callUpdateExchangeRatesMethod({
                 allTokens: {
-                  [toHex(1)]: {
+                  [ChainId.mainnet]: {
                     [controller.config.selectedAddress]: [
                       {
                         address: tokenAddress,
@@ -1700,11 +1759,12 @@ describe('TokenRatesController', () => {
                     ],
                   },
                 },
-                chainId: toHex(1),
+                chainId: ChainId.mainnet,
                 controller,
                 controllerEvents,
                 method,
                 nativeCurrency: 'ETH',
+                selectedNetworkClientId: InfuraNetworkType.mainnet,
               }),
           ).rejects.toThrow('Failed to fetch');
           expect(controller.state.contractExchangeRates).toStrictEqual({});
@@ -1716,7 +1776,7 @@ describe('TokenRatesController', () => {
     });
 
     it('fetches rates for all tokens in batches', async () => {
-      const chainId = toHex(1);
+      const chainId = ChainId.mainnet;
       const ticker = 'ETH';
       const tokenAddresses = [...new Array(200).keys()]
         .map(buildAddress)
@@ -1750,6 +1810,7 @@ describe('TokenRatesController', () => {
             controllerEvents,
             method,
             nativeCurrency: ticker,
+            selectedNetworkClientId: InfuraNetworkType.mainnet,
           });
 
           const numBatches = Math.ceil(
@@ -1795,7 +1856,7 @@ describe('TokenRatesController', () => {
         async ({ controller, controllerEvents }) => {
           await callUpdateExchangeRatesMethod({
             allTokens: {
-              [toHex(1)]: {
+              [ChainId.mainnet]: {
                 [controller.config.selectedAddress]: [
                   {
                     address: tokenAddresses[0],
@@ -1812,11 +1873,12 @@ describe('TokenRatesController', () => {
                 ],
               },
             },
-            chainId: toHex(1),
+            chainId: ChainId.mainnet,
             controller,
             controllerEvents,
             method,
             nativeCurrency: 'ETH',
+            selectedNetworkClientId: InfuraNetworkType.mainnet,
           });
 
           expect(controller.state).toMatchInlineSnapshot(`
@@ -1908,6 +1970,12 @@ describe('TokenRatesController', () => {
     }
 
     it('updates exchange rates when native currency is not supported by the Price API', async () => {
+      const selectedNetworkClientId = 'AAAA-BBBB-CCCC-DDDD';
+      const selectedNetworkClientConfiguration =
+        buildCustomNetworkClientConfiguration({
+          chainId: toHex(137),
+          ticker: 'UNSUPPORTED',
+        });
       const tokenAddresses = [
         '0x0000000000000000000000000000000000000001',
         '0x0000000000000000000000000000000000000002',
@@ -1935,16 +2003,23 @@ describe('TokenRatesController', () => {
         .get('/data/price')
         .query({
           fsym: 'ETH',
-          tsyms: 'UNSUPPORTED',
+          tsyms: selectedNetworkClientConfiguration.ticker,
         })
-        .reply(200, { UNSUPPORTED: 0.5 }); // .5 eth to 1 matic
+        .reply(200, { [selectedNetworkClientConfiguration.ticker]: 0.5 }); // .5 eth to 1 matic
 
       await withController(
-        { options: { tokenPricesService } },
+        {
+          options: {
+            tokenPricesService,
+          },
+          mockNetworkClientConfigurationsByNetworkClientId: {
+            [selectedNetworkClientId]: selectedNetworkClientConfiguration,
+          },
+        },
         async ({ controller, controllerEvents }) => {
           await callUpdateExchangeRatesMethod({
             allTokens: {
-              [toHex(137)]: {
+              [selectedNetworkClientConfiguration.chainId]: {
                 [controller.config.selectedAddress]: [
                   {
                     address: tokenAddresses[0],
@@ -1961,11 +2036,12 @@ describe('TokenRatesController', () => {
                 ],
               },
             },
-            chainId: toHex(137),
+            chainId: selectedNetworkClientConfiguration.chainId,
             controller,
             controllerEvents,
             method,
-            nativeCurrency: 'UNSUPPORTED',
+            nativeCurrency: selectedNetworkClientConfiguration.ticker,
+            selectedNetworkClientId,
           });
 
           // token value in terms of matic should be (token value in eth) * (eth value in matic)
@@ -1990,15 +2066,19 @@ describe('TokenRatesController', () => {
     });
 
     it('fetches rates for all tokens in batches when native currency is not supported by the Price API', async () => {
-      const chainId = toHex(1);
-      const ticker = 'UNSUPPORTED';
+      const selectedNetworkClientId = 'AAAA-BBBB-CCCC-DDDD';
+      const selectedNetworkClientConfiguration =
+        buildCustomNetworkClientConfiguration({
+          chainId: toHex(999),
+          ticker: 'UNSUPPORTED',
+        });
       const tokenAddresses = [...new Array(200).keys()]
         .map(buildAddress)
         .sort();
       const tokenPricesService = buildMockTokenPricesService({
         fetchTokenPrices: fetchTokenPricesWithIncreasingPriceForEachToken,
         validateCurrencySupported: (currency: unknown): currency is string => {
-          return currency !== ticker;
+          return currency !== selectedNetworkClientConfiguration.ticker;
         },
       });
       const fetchTokenPricesSpy = jest.spyOn(
@@ -2012,28 +2092,31 @@ describe('TokenRatesController', () => {
         .get('/data/price')
         .query({
           fsym: 'ETH',
-          tsyms: ticker,
+          tsyms: selectedNetworkClientConfiguration.ticker,
         })
-        .reply(200, { [ticker]: 0.5 });
+        .reply(200, { [selectedNetworkClientConfiguration.ticker]: 0.5 });
       await withController(
         {
           options: {
-            ticker,
             tokenPricesService,
           },
+          mockNetworkClientConfigurationsByNetworkClientId: {
+            [selectedNetworkClientId]: selectedNetworkClientConfiguration,
+          },
         },
         async ({ controller, controllerEvents }) => {
           await callUpdateExchangeRatesMethod({
             allTokens: {
-              [chainId]: {
+              [selectedNetworkClientConfiguration.chainId]: {
                 [controller.config.selectedAddress]: tokens,
               },
             },
-            chainId,
+            chainId: selectedNetworkClientConfiguration.chainId,
             controller,
             controllerEvents,
             method,
-            nativeCurrency: ticker,
+            nativeCurrency: selectedNetworkClientConfiguration.ticker,
+            selectedNetworkClientId,
           });
 
           const numBatches = Math.ceil(
@@ -2043,7 +2126,7 @@ describe('TokenRatesController', () => {
 
           for (let i = 1; i <= numBatches; i++) {
             expect(fetchTokenPricesSpy).toHaveBeenNthCalledWith(i, {
-              chainId,
+              chainId: selectedNetworkClientConfiguration.chainId,
               tokenAddresses: tokenAddresses.slice(
                 (i - 1) * TOKEN_PRICES_BATCH_SIZE,
                 i * TOKEN_PRICES_BATCH_SIZE,
@@ -2056,6 +2139,12 @@ describe('TokenRatesController', () => {
     });
 
     it('sets rates to undefined when chain is not supported by the Price API', async () => {
+      const selectedNetworkClientId = 'AAAA-BBBB-CCCC-DDDD';
+      const selectedNetworkClientConfiguration =
+        buildCustomNetworkClientConfiguration({
+          chainId: toHex(999),
+          ticker: 'TST',
+        });
       const tokenAddresses = [
         '0x0000000000000000000000000000000000000001',
         '0x0000000000000000000000000000000000000002',
@@ -2080,11 +2169,18 @@ describe('TokenRatesController', () => {
         ) as unknown as AbstractTokenPricesService['validateChainIdSupported'],
       });
       await withController(
-        { options: { tokenPricesService } },
+        {
+          options: {
+            tokenPricesService,
+          },
+          mockNetworkClientConfigurationsByNetworkClientId: {
+            [selectedNetworkClientId]: selectedNetworkClientConfiguration,
+          },
+        },
         async ({ controller, controllerEvents }) => {
           await callUpdateExchangeRatesMethod({
             allTokens: {
-              [toHex(999)]: {
+              [selectedNetworkClientConfiguration.chainId]: {
                 [controller.config.selectedAddress]: [
                   {
                     address: tokenAddresses[0],
@@ -2101,11 +2197,12 @@ describe('TokenRatesController', () => {
                 ],
               },
             },
-            chainId: toHex(999),
+            chainId: selectedNetworkClientConfiguration.chainId,
             controller,
             controllerEvents,
             method,
-            nativeCurrency: 'TST',
+            nativeCurrency: selectedNetworkClientConfiguration.ticker,
+            selectedNetworkClientId,
           });
 
           expect(controller.state).toMatchInlineSnapshot(`
@@ -2171,7 +2268,8 @@ describe('TokenRatesController', () => {
                   ],
                 },
               },
-              chainId: toHex(1),
+              chainId: ChainId.mainnet,
+              selectedNetworkClientId: InfuraNetworkType.mainnet,
               controller,
               controllerEvents,
               method,
@@ -2232,6 +2330,10 @@ type PartialConstructorParameters = {
   options?: Partial<ConstructorParameters<typeof TokenRatesController>[0]>;
   config?: Partial<TokenRatesConfig>;
   state?: Partial<TokenRatesState>;
+  mockNetworkClientConfigurationsByNetworkClientId?: Record<
+    NetworkClientId,
+    NetworkClientConfiguration
+  >;
 };
 
 type WithControllerArgs<ReturnValue> =
@@ -2250,20 +2352,29 @@ type WithControllerArgs<ReturnValue> =
 async function withController<ReturnValue>(
   ...args: WithControllerArgs<ReturnValue>
 ) {
-  const [{ options, config, state }, testFunction] =
-    args.length === 2
-      ? args
-      : [{ options: undefined, config: undefined, state: undefined }, args[0]];
+  const [
+    {
+      options = {},
+      config = {},
+      state = {},
+      mockNetworkClientConfigurationsByNetworkClientId = {},
+    },
+    testFunction,
+  ] = args.length === 2 ? args : [{}, args[0]];
 
   // explit cast used here because we know the `on____` functions are always
   // set in the constructor.
   const controllerEvents = {} as ControllerEvents;
 
+  const getNetworkClientById = buildMockGetNetworkClientById(
+    mockNetworkClientConfigurationsByNetworkClientId,
+  );
+
   const controllerOptions: ConstructorParameters<
     typeof TokenRatesController
   >[0] = {
     chainId: toHex(1),
-    getNetworkClientById: jest.fn(),
+    getNetworkClientById,
     onNetworkStateChange: (listener) => {
       controllerEvents.networkStateChange = listener;
     },
@@ -2315,6 +2426,8 @@ async function withController<ReturnValue>(
  * network we're getting updated exchange rates for.
  * @param args.setChainAsCurrent - When calling `updateExchangeRatesByChainId`,
  * this determines whether to set the chain as the globally selected chain.
+ * @param args.selectedNetworkClientId - The network client ID to use if
+ * `setChainAsCurrent` is true.
  */
 async function callUpdateExchangeRatesMethod({
   allTokens,
@@ -2323,14 +2436,16 @@ async function callUpdateExchangeRatesMethod({
   controllerEvents,
   method,
   nativeCurrency,
+  selectedNetworkClientId,
   setChainAsCurrent = true,
 }: {
   allTokens: TokenRatesConfig['allTokens'];
-  chainId: TokenRatesConfig['chainId'];
+  chainId: Hex;
   controller: TokenRatesController;
   controllerEvents: ControllerEvents;
   method: 'updateExchangeRates' | 'updateExchangeRatesByChainId';
   nativeCurrency: TokenRatesConfig['nativeCurrency'];
+  selectedNetworkClientId?: NetworkClientId;
   setChainAsCurrent?: boolean;
 }) {
   if (method === 'updateExchangeRates' && !setChainAsCurrent) {
@@ -2346,17 +2461,22 @@ async function callUpdateExchangeRatesMethod({
   controllerEvents.tokensStateChange({ allDetectedTokens: {}, allTokens });
 
   if (setChainAsCurrent) {
+    assert(
+      selectedNetworkClientId,
+      'The "selectedNetworkClientId" option must be given if the "setChainAsCurrent" flag is also given',
+    );
+
     // We're using controller events here instead of calling `configure`
     // because `configure` does not update internal controller state correctly.
     // As with many BaseControllerV1-based controllers, runtime config
     // modification is allowed by the API but not supported in practice.
+    //
+    // @ts-expect-error Note that the state given here is intentionally
+    // incomplete because the controller only uses this one property, and the
+    // tests are written to only consider it. We want this to break if we start
+    // relying on more properties, as we'd need to update the tests accordingly.
     controllerEvents.networkStateChange({
-      // Note that the state given here is intentionally incomplete because the
-      // controller only uses these two properties, and the tests are written to
-      // only consider these two. We want this to break if we start relying on
-      // more, as we'd need to update the tests accordingly.
-      // @ts-expect-error Intentionally incomplete state
-      providerConfig: { chainId, ticker: nativeCurrency },
+      selectedNetworkClientId,
     });
   }
 
diff --git a/packages/assets-controllers/src/TokenRatesController.ts b/packages/assets-controllers/src/TokenRatesController.ts
index 099e500004..a564e8b5a0 100644
--- a/packages/assets-controllers/src/TokenRatesController.ts
+++ b/packages/assets-controllers/src/TokenRatesController.ts
@@ -254,8 +254,12 @@ export class TokenRatesController extends StaticIntervalPollingControllerV1<
       }
     });
 
-    onNetworkStateChange(async ({ providerConfig }) => {
-      const { chainId, ticker } = providerConfig;
+    onNetworkStateChange(async ({ selectedNetworkClientId }) => {
+      const selectedNetworkClient = getNetworkClientById(
+        selectedNetworkClientId,
+      );
+      const { chainId, ticker } = selectedNetworkClient.configuration;
+
       if (
         this.config.chainId !== chainId ||
         this.config.nativeCurrency !== ticker