diff --git a/spec/integ/crypto/rust-crypto.spec.ts b/spec/integ/crypto/rust-crypto.spec.ts
index 311410febbe..c6b990fed0f 100644
--- a/spec/integ/crypto/rust-crypto.spec.ts
+++ b/spec/integ/crypto/rust-crypto.spec.ts
@@ -85,6 +85,44 @@ describe("MatrixClient.initRustCrypto", () => {
         );
     });
 
+    it("should create the meta db if given a storageKey", async () => {
+        const matrixClient = createClient({
+            baseUrl: "http://test.server",
+            userId: "@alice:localhost",
+            deviceId: "aliceDevice",
+        });
+
+        // No databases.
+        expect(await indexedDB.databases()).toHaveLength(0);
+
+        await matrixClient.initRustCrypto({ storageKey: new Uint8Array(32) });
+
+        // should have two indexed dbs now
+        const databaseNames = (await indexedDB.databases()).map((db) => db.name);
+        expect(databaseNames).toEqual(
+            expect.arrayContaining(["matrix-js-sdk::matrix-sdk-crypto", "matrix-js-sdk::matrix-sdk-crypto-meta"]),
+        );
+    });
+
+    it("should create the meta db if given a storagePassword", async () => {
+        const matrixClient = createClient({
+            baseUrl: "http://test.server",
+            userId: "@alice:localhost",
+            deviceId: "aliceDevice",
+        });
+
+        // No databases.
+        expect(await indexedDB.databases()).toHaveLength(0);
+
+        await matrixClient.initRustCrypto({ storagePassword: "the cow is on the moon" });
+
+        // should have two indexed dbs now
+        const databaseNames = (await indexedDB.databases()).map((db) => db.name);
+        expect(databaseNames).toEqual(
+            expect.arrayContaining(["matrix-js-sdk::matrix-sdk-crypto", "matrix-js-sdk::matrix-sdk-crypto-meta"]),
+        );
+    });
+
     it("should ignore a second call", async () => {
         const matrixClient = createClient({
             baseUrl: "http://test.server",
diff --git a/spec/unit/rust-crypto/rust-crypto.spec.ts b/spec/unit/rust-crypto/rust-crypto.spec.ts
index c6507a0d145..90cd079912e 100644
--- a/spec/unit/rust-crypto/rust-crypto.spec.ts
+++ b/spec/unit/rust-crypto/rust-crypto.spec.ts
@@ -104,7 +104,7 @@ describe("initRustCrypto", () => {
         } as unknown as Mocked<OlmMachine>;
     }
 
-    it("passes through the store params", async () => {
+    it("passes through the store params (passphrase)", async () => {
         const mockStore = { free: jest.fn() } as unknown as StoreHandle;
         jest.spyOn(StoreHandle, "open").mockResolvedValue(mockStore);
 
@@ -126,7 +126,30 @@ describe("initRustCrypto", () => {
         expect(OlmMachine.initFromStore).toHaveBeenCalledWith(expect.anything(), expect.anything(), mockStore);
     });
 
-    it("suppresses the storePassphrase if storePrefix is unset", async () => {
+    it("passes through the store params (key)", async () => {
+        const mockStore = { free: jest.fn() } as unknown as StoreHandle;
+        jest.spyOn(StoreHandle, "openWithKey").mockResolvedValue(mockStore);
+
+        const testOlmMachine = makeTestOlmMachine();
+        jest.spyOn(OlmMachine, "initFromStore").mockResolvedValue(testOlmMachine);
+
+        const storeKey = new Uint8Array(32);
+        await initRustCrypto({
+            logger,
+            http: {} as MatrixClient["http"],
+            userId: TEST_USER,
+            deviceId: TEST_DEVICE_ID,
+            secretStorage: {} as ServerSideSecretStorage,
+            cryptoCallbacks: {} as CryptoCallbacks,
+            storePrefix: "storePrefix",
+            storeKey: storeKey,
+        });
+
+        expect(StoreHandle.openWithKey).toHaveBeenCalledWith("storePrefix", storeKey);
+        expect(OlmMachine.initFromStore).toHaveBeenCalledWith(expect.anything(), expect.anything(), mockStore);
+    });
+
+    it("suppresses the storePassphrase and storeKey if storePrefix is unset", async () => {
         const mockStore = { free: jest.fn() } as unknown as StoreHandle;
         jest.spyOn(StoreHandle, "open").mockResolvedValue(mockStore);
 
@@ -141,10 +164,11 @@ describe("initRustCrypto", () => {
             secretStorage: {} as ServerSideSecretStorage,
             cryptoCallbacks: {} as CryptoCallbacks,
             storePrefix: null,
+            storeKey: new Uint8Array(),
             storePassphrase: "storePassphrase",
         });
 
-        expect(StoreHandle.open).toHaveBeenCalledWith(undefined, undefined);
+        expect(StoreHandle.open).toHaveBeenCalledWith();
         expect(OlmMachine.initFromStore).toHaveBeenCalledWith(expect.anything(), expect.anything(), mockStore);
     });
 
diff --git a/src/client.ts b/src/client.ts
index 27485d076f8..2e349213123 100644
--- a/src/client.ts
+++ b/src/client.ts
@@ -357,14 +357,14 @@ export interface ICreateClientOpts {
     deviceToImport?: IExportedDevice;
 
     /**
-     * Encryption key used for encrypting sensitive data (such as e2ee keys) in storage.
+     * Encryption key used for encrypting sensitive data (such as e2ee keys) in {@link ICreateClientOpts#cryptoStore}.
      *
      * This must be set to the same value every time the client is initialised for the same device.
      *
-     * If unset, either a hardcoded key or no encryption at all is used, depending on the Crypto implementation.
-     *
-     * No particular requirement is placed on the key data (it is fed into an HKDF to generate the actual encryption
-     * keys).
+     * This is only used for the legacy crypto implementation (as used by {@link MatrixClient#initCrypto}),
+     * but if you use the rust crypto implementation ({@link MatrixClient#initRustCrypto}) and the device
+     * previously used legacy crypto (so must be migrated), then this must still be provided, so that the
+     * data can be migrated from the legacy store.
      */
     pickleKey?: string;
 
@@ -2229,17 +2229,24 @@ export class MatrixClient extends TypedEventEmitter<EmittedEvents, ClientEventHa
      *
      * An alternative to {@link initCrypto}.
      *
-     * *WARNING*: this API is very experimental, should not be used in production, and may change without notice!
-     *    Eventually it will be deprecated and `initCrypto` will do the same thing.
-     *
-     * @experimental
-     *
-     * @param useIndexedDB - True to use an indexeddb store, false to use an in-memory store. Defaults to 'true'.
+     * @param args.useIndexedDB - True to use an indexeddb store, false to use an in-memory store. Defaults to 'true'.
+     * @param args.storageKey - A key with which to encrypt the indexeddb store. If provided, it must be exactly
+     *    32 bytes of data, and must be the same each time the client is initialised for a given device.
+     *    If both this and `storagePassword` are unspecified, the store will be unencrypted.
+     * @param args.storagePassword - An alternative to `storageKey`. A password which will be used to derive a key to
+     *    encrypt the store with. Deriving a key from a password is (deliberately) a slow operation, so prefer
+     *    to pass a `storageKey` directly where possible.
      *
      * @returns a Promise which will resolve when the crypto layer has been
      *    successfully initialised.
      */
-    public async initRustCrypto({ useIndexedDB = true }: { useIndexedDB?: boolean } = {}): Promise<void> {
+    public async initRustCrypto(
+        args: {
+            useIndexedDB?: boolean;
+            storageKey?: Uint8Array;
+            storagePassword?: string;
+        } = {},
+    ): Promise<void> {
         if (this.cryptoBackend) {
             this.logger.warn("Attempt to re-initialise e2e encryption on MatrixClient");
             return;
@@ -2272,11 +2279,15 @@ export class MatrixClient extends TypedEventEmitter<EmittedEvents, ClientEventHa
             deviceId: deviceId,
             secretStorage: this.secretStorage,
             cryptoCallbacks: this.cryptoCallbacks,
-            storePrefix: useIndexedDB ? RUST_SDK_STORE_PREFIX : null,
-            storePassphrase: this.pickleKey,
+            storePrefix: args.useIndexedDB === false ? null : RUST_SDK_STORE_PREFIX,
+            storeKey: args.storageKey,
+
+            // temporary compatibility hack: if there is no storageKey nor storagePassword, fall back to the pickleKey
+            storePassphrase: args.storagePassword ?? this.pickleKey,
+
             legacyCryptoStore: this.cryptoStore,
             legacyPickleKey: this.pickleKey ?? "DEFAULT_KEY",
-            legacyMigrationProgressListener: (progress, total) => {
+            legacyMigrationProgressListener: (progress: number, total: number): void => {
                 this.emit(CryptoEvent.LegacyCryptoStoreMigrationProgress, progress, total);
             },
         });
diff --git a/src/rust-crypto/index.ts b/src/rust-crypto/index.ts
index 6defede1e95..dc9a42af743 100644
--- a/src/rust-crypto/index.ts
+++ b/src/rust-crypto/index.ts
@@ -64,13 +64,21 @@ export async function initRustCrypto(args: {
     storePrefix: string | null;
 
     /**
-     * A passphrase to use to encrypt the indexeddbs created by rust-crypto.
+     * A passphrase to use to encrypt the indexeddb created by rust-crypto.
      *
-     * Ignored if `storePrefix` is null. If this is `undefined` (and `storePrefix` is not null), the indexeddbs
-     * will be unencrypted.
+     * Ignored if `storePrefix` is null, or `storeKey` is set.  If neither this nor `storeKey` is set
+     * (and `storePrefix` is not null), the indexeddb will be unencrypted.
      */
     storePassphrase?: string;
 
+    /**
+     * A key to use to encrypt the indexeddb created by rust-crypto.
+     *
+     * Ignored if `storePrefix` is null. Otherwise, if it is set, it must be a 32-byte cryptographic key, which
+     * will be used to encrypt the indexeddb. See also `storePassphrase`.
+     */
+    storeKey?: Uint8Array;
+
     /** If defined, we will check if any data needs migrating from this store to the rust store. */
     legacyCryptoStore?: CryptoStore;
 
@@ -94,10 +102,16 @@ export async function initRustCrypto(args: {
     new RustSdkCryptoJs.Tracing(RustSdkCryptoJs.LoggerLevel.Debug).turnOn();
 
     logger.debug("Opening Rust CryptoStore");
-    const storeHandle: StoreHandle = await StoreHandle.open(
-        args.storePrefix ?? undefined,
-        (args.storePrefix && args.storePassphrase) ?? undefined,
-    );
+    let storeHandle;
+    if (args.storePrefix) {
+        if (args.storeKey) {
+            storeHandle = await StoreHandle.openWithKey(args.storePrefix, args.storeKey);
+        } else {
+            storeHandle = await StoreHandle.open(args.storePrefix, args.storePassphrase);
+        }
+    } else {
+        storeHandle = await StoreHandle.open();
+    }
 
     if (args.legacyCryptoStore) {
         // We have a legacy crypto store, which we may need to migrate from.