diff --git a/api/custom_auth/oauth/serializers.py b/api/custom_auth/oauth/serializers.py
index 63e758b127bf..6a1e80ab90af 100644
--- a/api/custom_auth/oauth/serializers.py
+++ b/api/custom_auth/oauth/serializers.py
@@ -1,11 +1,15 @@
+from abc import abstractmethod
+
 from django.conf import settings
 from django.contrib.auth import get_user_model
 from django.contrib.auth.signals import user_logged_in
+from django.db.models import F
 from rest_framework import serializers
 from rest_framework.authtoken.models import Token
 from rest_framework.exceptions import PermissionDenied
 
 from organisations.invites.models import Invite
+from users.auth_type import AuthType
 from users.models import SignUpType
 
 from ..constants import USER_REGISTRATION_WITHOUT_INVITE_ERROR_MESSAGE
@@ -30,6 +34,9 @@ class OAuthLoginSerializer(serializers.Serializer):
         write_only=True,
     )
 
+    auth_type: AuthType | None = None
+    user_model_id_attribute: str = "id"
+
     class Meta:
         abstract = True
 
@@ -53,8 +60,28 @@ def create(self, validated_data):
         return Token.objects.get_or_create(user=user)[0]
 
     def _get_user(self, user_data: dict):
-        email = user_data.get("email")
-        existing_user = UserModel.objects.filter(email=email).first()
+        email: str = user_data.pop("email")
+
+        # There are a number of scenarios that we're catering for in this
+        # query:
+        #  1. A new user arriving, and immediately authenticating with
+        #     the given social auth method.
+        #  2. A user that has previously authenticated with method A is now
+        #     authenticating with method B. Using the `email__iexact` means
+        #     that we'll always retrieve the user that already authenticated
+        #     with A.
+        #  3. A user that (prior to the case sensitivity fix) authenticated
+        #     with multiple methods and ended up with duplicate user accounts.
+        #     Since it's difficult for us to know which user account they are
+        #     using as their primary, we order by the method they are currently
+        #     authenticating with and grab the first one in the list.
+        existing_user = (
+            UserModel.objects.filter(email__iexact=email)
+            .order_by(
+                F(self.user_model_id_attribute).desc(nulls_last=True),
+            )
+            .first()
+        )
 
         if not existing_user:
             sign_up_type = self.validated_data.get("sign_up_type")
@@ -65,20 +92,46 @@ def _get_user(self, user_data: dict):
             ):
                 raise PermissionDenied(USER_REGISTRATION_WITHOUT_INVITE_ERROR_MESSAGE)
 
-            return UserModel.objects.create(**user_data, sign_up_type=sign_up_type)
+            return UserModel.objects.create(
+                **user_data, email=email.lower(), sign_up_type=sign_up_type
+            )
+        elif existing_user.auth_type != self.get_auth_type().value:
+            # In this scenario, we're seeing a user that had previously
+            # authenticated with another authentication method and is now
+            # authenticating with a new OAuth provider.
+            setattr(
+                existing_user,
+                self.user_model_id_attribute,
+                user_data[self.user_model_id_attribute],
+            )
+            existing_user.save()
 
         return existing_user
 
+    @abstractmethod
     def get_user_info(self):
         raise NotImplementedError("`get_user_info()` must be implemented.")
 
+    def get_auth_type(self) -> AuthType:
+        if not self.auth_type:  # pragma: no cover
+            raise NotImplementedError(
+                "`auth_type` must be set, or `get_auth_type()` must be implemented."
+            )
+        return self.auth_type
+
 
 class GoogleLoginSerializer(OAuthLoginSerializer):
+    auth_type = AuthType.GOOGLE
+    user_model_id_attribute = "google_user_id"
+
     def get_user_info(self):
         return get_user_info(self.validated_data["access_token"])
 
 
 class GithubLoginSerializer(OAuthLoginSerializer):
+    auth_type = AuthType.GITHUB
+    user_model_id_attribute = "github_user_id"
+
     def get_user_info(self):
         github_user = GithubUser(code=self.validated_data["access_token"])
         return github_user.get_user_info()
diff --git a/api/tests/unit/custom_auth/oauth/test_unit_oauth_views.py b/api/tests/unit/custom_auth/oauth/test_unit_oauth_views.py
index 2a8895de490c..0f742267b71b 100644
--- a/api/tests/unit/custom_auth/oauth/test_unit_oauth_views.py
+++ b/api/tests/unit/custom_auth/oauth/test_unit_oauth_views.py
@@ -1,7 +1,9 @@
 from unittest import mock
 
+from django.db.models import Model
 from django.test import override_settings
 from django.urls import reverse
+from pytest_mock import MockerFixture
 from rest_framework import status
 from rest_framework.test import APIClient
 
@@ -103,7 +105,12 @@ def test_can_login_with_google_if_registration_disabled(
     client = APIClient()
 
     email = "test@example.com"
-    mock_get_user_info.return_value = {"email": email}
+    mock_get_user_info.return_value = {
+        "email": email,
+        "first_name": "John",
+        "last_name": "Smith",
+        "google_user_id": "abc123",
+    }
     django_user_model.objects.create(email=email)
 
     # When
@@ -126,7 +133,12 @@ def test_can_login_with_github_if_registration_disabled(
     email = "test@example.com"
     mock_github_user = mock.MagicMock()
     MockGithubUser.return_value = mock_github_user
-    mock_github_user.get_user_info.return_value = {"email": email}
+    mock_github_user.get_user_info.return_value = {
+        "email": email,
+        "first_name": "John",
+        "last_name": "Smith",
+        "github_user_id": "abc123",
+    }
     django_user_model.objects.create(email=email)
 
     # When
@@ -135,3 +147,144 @@ def test_can_login_with_github_if_registration_disabled(
     # Then
     assert response.status_code == status.HTTP_200_OK
     assert "key" in response.json()
+
+
+def test_login_with_google_updates_existing_user_case_insensitive(
+    db: None,
+    django_user_model: type[Model],
+    mocker: MockerFixture,
+    api_client: APIClient,
+) -> None:
+    # Given
+    email_lower = "test@example.com"
+    email_upper = email_lower.upper()
+    google_user_id = "abc123"
+
+    django_user_model.objects.create(email=email_lower)
+
+    mocker.patch(
+        "custom_auth.oauth.serializers.get_user_info",
+        return_value={
+            "email": email_upper,
+            "first_name": "John",
+            "last_name": "Smith",
+            "google_user_id": google_user_id,
+        },
+    )
+
+    url = reverse("api-v1:custom_auth:oauth:google-oauth-login")
+
+    # When
+    response = api_client.post(url, data={"access_token": "some-token"})
+
+    # Then
+    assert response.status_code == status.HTTP_200_OK
+
+    qs = django_user_model.objects.filter(email__iexact=email_lower)
+    assert qs.count() == 1
+
+    user = qs.first()
+    assert user.email == email_lower
+    assert user.google_user_id == google_user_id
+
+
+def test_login_with_github_updates_existing_user_case_insensitive(
+    db: None,
+    django_user_model: type[Model],
+    mocker: MockerFixture,
+    api_client: APIClient,
+) -> None:
+    # Given
+    email_lower = "test@example.com"
+    email_upper = email_lower.upper()
+    github_user_id = "abc123"
+
+    django_user_model.objects.create(email=email_lower)
+
+    mock_github_user = mock.MagicMock()
+    mocker.patch(
+        "custom_auth.oauth.serializers.GithubUser", return_value=mock_github_user
+    )
+    mock_github_user.get_user_info.return_value = {
+        "email": email_upper,
+        "first_name": "John",
+        "last_name": "Smith",
+        "github_user_id": github_user_id,
+    }
+
+    url = reverse("api-v1:custom_auth:oauth:github-oauth-login")
+
+    # When
+    response = api_client.post(url, data={"access_token": "some-token"})
+
+    # Then
+    assert response.status_code == status.HTTP_200_OK
+
+    qs = django_user_model.objects.filter(email__iexact=email_lower)
+    assert qs.count() == 1
+
+    user = qs.first()
+    assert user.email == email_lower
+    assert user.github_user_id == github_user_id
+
+
+def test_user_with_duplicate_accounts_authenticates_as_the_correct_oauth_user(
+    db: None,
+    django_user_model: type[Model],
+    api_client: APIClient,
+    mocker: MockerFixture,
+) -> None:
+    """
+    Specific test to verify the correct behaviour for users affected by
+    https://github.com/Flagsmith/flagsmith/issues/4185.
+    """
+
+    # Given
+    email_lower = "test@example.com"
+    email_upper = email_lower.upper()
+
+    github_user = django_user_model.objects.create(
+        email=email_lower, github_user_id="abc123"
+    )
+    google_user = django_user_model.objects.create(
+        email=email_upper, google_user_id="abc123"
+    )
+
+    mock_github_user = mock.MagicMock()
+    mocker.patch(
+        "custom_auth.oauth.serializers.GithubUser", return_value=mock_github_user
+    )
+    mock_github_user.get_user_info.return_value = {
+        "email": email_lower,
+        "first_name": "John",
+        "last_name": "Smith",
+        "github_user_id": github_user.github_user_id,
+    }
+
+    mocker.patch(
+        "custom_auth.oauth.serializers.get_user_info",
+        return_value={
+            "email": email_upper,
+            "first_name": "John",
+            "last_name": "Smith",
+            "google_user_id": google_user.google_user_id,
+        },
+    )
+
+    github_auth_url = reverse("api-v1:custom_auth:oauth:github-oauth-login")
+    google_auth_url = reverse("api-v1:custom_auth:oauth:google-oauth-login")
+
+    # When
+    auth_with_github_response = api_client.post(
+        github_auth_url, data={"access_token": "some-token"}
+    )
+    auth_with_google_response = api_client.post(
+        google_auth_url, data={"access_token": "some-token"}
+    )
+
+    # Then
+    github_auth_key = auth_with_github_response.json().get("key")
+    assert github_auth_key == github_user.auth_token.key
+
+    google_auth_key = auth_with_google_response.json().get("key")
+    assert google_auth_key == google_user.auth_token.key