diff --git a/cypress/e2e/register/register.spec.ts b/cypress/e2e/register/register.spec.ts
index 8d1076f0b78..a0c120414d2 100644
--- a/cypress/e2e/register/register.spec.ts
+++ b/cypress/e2e/register/register.spec.ts
@@ -85,4 +85,48 @@ describe("Registration", () => {
         cy.get(".mx_DevicesPanel_myDevice .mx_DevicesPanel_deviceTrust .mx_E2EIcon")
             .should("have.class", "mx_E2EIcon_verified");
     });
+
+    it("should require username to fulfil requirements and be available", () => {
+        cy.get(".mx_ServerPicker_change", { timeout: 15000 }).click();
+        cy.get(".mx_ServerPickerDialog_continue").should("be.visible");
+        cy.get(".mx_ServerPickerDialog_otherHomeserver").type(synapse.baseUrl);
+        cy.get(".mx_ServerPickerDialog_continue").click();
+        // wait for the dialog to go away
+        cy.get('.mx_ServerPickerDialog').should('not.exist');
+
+        cy.get("#mx_RegistrationForm_username").should("be.visible");
+
+        cy.intercept("**/_matrix/client/*/register/available?username=_alice", {
+            statusCode: 400,
+            headers: {
+                "Content-Type": "application/json",
+            },
+            body: {
+                errcode: "M_INVALID_USERNAME",
+                error: "User ID may not begin with _",
+            },
+        });
+        cy.get("#mx_RegistrationForm_username").type("_alice");
+        cy.get(".mx_Field_tooltip")
+            .should("have.class", "mx_Tooltip_visible")
+            .should("contain.text", "Some characters not allowed");
+
+        cy.intercept("**/_matrix/client/*/register/available?username=bob", {
+            statusCode: 400,
+            headers: {
+                "Content-Type": "application/json",
+            },
+            body: {
+                errcode: "M_USER_IN_USE",
+                error: "The desired username is already taken",
+            },
+        });
+        cy.get("#mx_RegistrationForm_username").type("{selectAll}{backspace}bob");
+        cy.get(".mx_Field_tooltip")
+            .should("have.class", "mx_Tooltip_visible")
+            .should("contain.text", "Someone already has that username");
+
+        cy.get("#mx_RegistrationForm_username").type("{selectAll}{backspace}foobar");
+        cy.get(".mx_Field_tooltip").should("not.have.class", "mx_Tooltip_visible");
+    });
 });
diff --git a/src/components/views/auth/RegistrationForm.tsx b/src/components/views/auth/RegistrationForm.tsx
index 690acd5c318..d1f7c9acc45 100644
--- a/src/components/views/auth/RegistrationForm.tsx
+++ b/src/components/views/auth/RegistrationForm.tsx
@@ -18,6 +18,7 @@ limitations under the License.
 import React from 'react';
 import { MatrixClient } from 'matrix-js-sdk/src/client';
 import { logger } from "matrix-js-sdk/src/logger";
+import { MatrixError } from 'matrix-js-sdk/src/matrix';
 
 import * as Email from '../../../email';
 import { looksValid as phoneNumberLooksValid } from '../../../phonenumber';
@@ -48,6 +49,7 @@ enum UsernameAvailableStatus {
     Available,
     Unavailable,
     Error,
+    Invalid,
 }
 
 export const PASSWORD_MIN_SCORE = 3; // safely unguessable: moderate protection from offline slow-hash scenario.
@@ -363,6 +365,9 @@ export default class RegistrationForm extends React.PureComponent<IProps, IState
                 const available = await this.props.matrixClient.isUsernameAvailable(value);
                 return available ? UsernameAvailableStatus.Available : UsernameAvailableStatus.Unavailable;
             } catch (err) {
+                if (err instanceof MatrixError && err.errcode === "M_INVALID_USERNAME") {
+                    return UsernameAvailableStatus.Invalid;
+                }
                 return UsernameAvailableStatus.Error;
             }
         },
@@ -374,7 +379,8 @@ export default class RegistrationForm extends React.PureComponent<IProps, IState
             },
             {
                 key: "safeLocalpart",
-                test: ({ value }) => !value || SAFE_LOCALPART_REGEX.test(value),
+                test: ({ value }, usernameAvailable) => (!value || SAFE_LOCALPART_REGEX.test(value))
+                    && usernameAvailable !== UsernameAvailableStatus.Invalid,
                 invalid: () => _t("Some characters not allowed"),
             },
             {