diff --git a/src/Lifecycle.ts b/src/Lifecycle.ts
index 0f2435ffe8..1d6577ca39 100644
--- a/src/Lifecycle.ts
+++ b/src/Lifecycle.ts
@@ -23,7 +23,7 @@ import { InvalidStoreError } from "matrix-js-sdk/src/errors";
 import { IEncryptedPayload } from "matrix-js-sdk/src/crypto/aes";
 import { QueryDict } from "matrix-js-sdk/src/utils";
 import { logger } from "matrix-js-sdk/src/logger";
-import { MINIMUM_MATRIX_VERSION } from "matrix-js-sdk/src/version-support";
+import { MINIMUM_MATRIX_VERSION, SUPPORTED_MATRIX_VERSIONS } from "matrix-js-sdk/src/version-support";
 
 import { IMatrixClientCreds, MatrixClientPeg } from "./MatrixClientPeg";
 import SecurityCustomisations from "./customisations/Security";
@@ -635,7 +635,7 @@ export async function restoreFromLocalStorage(opts?: { ignoreGuest?: boolean }):
             },
             false,
         );
-        checkServerVersions();
+        await checkServerVersions();
         return true;
     } else {
         logger.log("No previous session found.");
@@ -644,29 +644,34 @@ export async function restoreFromLocalStorage(opts?: { ignoreGuest?: boolean }):
 }
 
 async function checkServerVersions(): Promise<void> {
-    MatrixClientPeg.get()
-        ?.getVersions()
-        .then((response) => {
-            if (!response.versions.includes(MINIMUM_MATRIX_VERSION)) {
-                const toastKey = "LEGACY_SERVER";
-                ToastStore.sharedInstance().addOrReplaceToast({
-                    key: toastKey,
-                    title: _t("unsupported_server_title"),
-                    props: {
-                        description: _t("unsupported_server_description", {
-                            version: MINIMUM_MATRIX_VERSION,
-                            brand: SdkConfig.get().brand,
-                        }),
-                        acceptLabel: _t("action|ok"),
-                        onAccept: () => {
-                            ToastStore.sharedInstance().dismissToast(toastKey);
-                        },
-                    },
-                    component: GenericToast,
-                    priority: 98,
-                });
-            }
-        });
+    const client = MatrixClientPeg.get();
+    if (!client) return;
+    for (const version of SUPPORTED_MATRIX_VERSIONS) {
+        // Check if the server supports this spec version. (`isVersionSupported` caches the response, so this loop will
+        // only make a single HTTP request).
+        if (await client.isVersionSupported(version)) {
+            // we found a compatible spec version
+            return;
+        }
+    }
+
+    const toastKey = "LEGACY_SERVER";
+    ToastStore.sharedInstance().addOrReplaceToast({
+        key: toastKey,
+        title: _t("unsupported_server_title"),
+        props: {
+            description: _t("unsupported_server_description", {
+                version: MINIMUM_MATRIX_VERSION,
+                brand: SdkConfig.get().brand,
+            }),
+            acceptLabel: _t("action|ok"),
+            onAccept: () => {
+                ToastStore.sharedInstance().dismissToast(toastKey);
+            },
+        },
+        component: GenericToast,
+        priority: 98,
+    });
 }
 
 async function handleLoadSessionFailure(e: unknown): Promise<boolean> {
diff --git a/test/Lifecycle-test.ts b/test/Lifecycle-test.ts
index b984549e9d..90dd0c5335 100644
--- a/test/Lifecycle-test.ts
+++ b/test/Lifecycle-test.ts
@@ -453,10 +453,7 @@ describe("Lifecycle", () => {
 
             it("should show a toast if the matrix server version is unsupported", async () => {
                 const toastSpy = jest.spyOn(ToastStore.sharedInstance(), "addOrReplaceToast");
-                mockClient.getVersions.mockResolvedValue({
-                    versions: ["r0.6.0"],
-                    unstable_features: {},
-                });
+                mockClient.isVersionSupported.mockImplementation(async (version) => version == "r0.6.0");
                 initLocalStorageMock({ ...localStorageSession });
 
                 expect(await restoreFromLocalStorage()).toEqual(true);