diff --git a/coderd/apidoc/docs.go b/coderd/apidoc/docs.go
index d58afadd533d9..9bf6444938c54 100644
--- a/coderd/apidoc/docs.go
+++ b/coderd/apidoc/docs.go
@@ -7044,7 +7044,6 @@ const docTemplate = `{
             "type": "object",
             "required": [
                 "email",
-                "organization_id",
                 "password",
                 "username"
             ],
diff --git a/coderd/apidoc/swagger.json b/coderd/apidoc/swagger.json
index dd75cdec2f03d..e82bf43527743 100644
--- a/coderd/apidoc/swagger.json
+++ b/coderd/apidoc/swagger.json
@@ -6262,7 +6262,7 @@
     },
     "codersdk.CreateUserRequest": {
       "type": "object",
-      "required": ["email", "organization_id", "password", "username"],
+      "required": ["email", "password", "username"],
       "properties": {
         "email": {
           "type": "string",
diff --git a/coderd/userauth.go b/coderd/userauth.go
index e3ee528e23e27..83c6be248a130 100644
--- a/coderd/userauth.go
+++ b/coderd/userauth.go
@@ -921,7 +921,11 @@ func (api *API) oauthLogin(r *http.Request, params oauthLoginParams) (*http.Cook
 					Username:       params.Username,
 					OrganizationID: organizationID,
 				},
-				LoginType: params.LoginType,
+				// All of the userauth tests depend on this being able to create
+				// the first organization. It shouldn't be possible in normal
+				// operation.
+				CreateOrganization: len(organizations) == 0,
+				LoginType:          params.LoginType,
 			})
 			if err != nil {
 				return xerrors.Errorf("create user: %w", err)
diff --git a/coderd/users.go b/coderd/users.go
index 44130cfbab940..205aa528b025b 100644
--- a/coderd/users.go
+++ b/coderd/users.go
@@ -128,7 +128,8 @@ func (api *API) postFirstUser(rw http.ResponseWriter, r *http.Request) {
 			// Create an org for the first user.
 			OrganizationID: uuid.Nil,
 		},
-		LoginType: database.LoginTypePassword,
+		CreateOrganization: true,
+		LoginType:          database.LoginTypePassword,
 	})
 	if err != nil {
 		httpapi.Write(ctx, rw, http.StatusInternalServerError, codersdk.Response{
@@ -313,19 +314,41 @@ func (api *API) postUser(rw http.ResponseWriter, r *http.Request) {
 		return
 	}
 
-	_, err = api.Database.GetOrganizationByID(ctx, req.OrganizationID)
-	if httpapi.Is404Error(err) {
-		httpapi.Write(ctx, rw, http.StatusNotFound, codersdk.Response{
-			Message: fmt.Sprintf("Organization does not exist with the provided id %q.", req.OrganizationID),
-		})
-		return
-	}
-	if err != nil {
-		httpapi.Write(ctx, rw, http.StatusInternalServerError, codersdk.Response{
-			Message: "Internal error fetching organization.",
-			Detail:  err.Error(),
-		})
-		return
+	if req.OrganizationID != uuid.Nil {
+		// If an organization was provided, make sure it exists.
+		_, err := api.Database.GetOrganizationByID(ctx, req.OrganizationID)
+		if err != nil {
+			if httpapi.Is404Error(err) {
+				httpapi.Write(ctx, rw, http.StatusNotFound, codersdk.Response{
+					Message: fmt.Sprintf("Organization does not exist with the provided id %q.", req.OrganizationID),
+				})
+				return
+			}
+
+			httpapi.Write(ctx, rw, http.StatusInternalServerError, codersdk.Response{
+				Message: "Internal error fetching organization.",
+				Detail:  err.Error(),
+			})
+			return
+		}
+	} else {
+		// If no organization is provided, add the user to the first
+		// organization.
+		organizations, err := api.Database.GetOrganizations(ctx)
+		if err != nil {
+			httpapi.Write(ctx, rw, http.StatusInternalServerError, codersdk.Response{
+				Message: "Internal error fetching orgs.",
+				Detail:  err.Error(),
+			})
+			return
+		}
+
+		if len(organizations) > 0 {
+			// Add the user to the first organization. Once multi-organization
+			// support is added, we should enable a configuration map of user
+			// email to organization.
+			req.OrganizationID = organizations[0].ID
+		}
 	}
 
 	err = userpassword.Validate(req.Password)
@@ -955,7 +978,8 @@ func (api *API) organizationByUserAndName(rw http.ResponseWriter, r *http.Reques
 
 type CreateUserRequest struct {
 	codersdk.CreateUserRequest
-	LoginType database.LoginType
+	CreateOrganization bool
+	LoginType          database.LoginType
 }
 
 func (api *API) CreateUser(ctx context.Context, store database.Store, req CreateUserRequest) (database.User, uuid.UUID, error) {
@@ -964,6 +988,10 @@ func (api *API) CreateUser(ctx context.Context, store database.Store, req Create
 		orgRoles := make([]string, 0)
 		// If no organization is provided, create a new one for the user.
 		if req.OrganizationID == uuid.Nil {
+			if !req.CreateOrganization {
+				return xerrors.Errorf("organization ID must be provided")
+			}
+
 			organization, err := tx.InsertOrganization(ctx, database.InsertOrganizationParams{
 				ID:        uuid.New(),
 				Name:      req.Username,
diff --git a/coderd/users_test.go b/coderd/users_test.go
index bd4bc77d580b7..053a86fd2be17 100644
--- a/coderd/users_test.go
+++ b/coderd/users_test.go
@@ -10,6 +10,7 @@ import (
 	"time"
 
 	"github.com/google/uuid"
+	"github.com/stretchr/testify/assert"
 	"github.com/stretchr/testify/require"
 	"golang.org/x/sync/errgroup"
 
@@ -478,21 +479,49 @@ func TestPostUsers(t *testing.T) {
 		require.Equal(t, http.StatusNotFound, apiErr.StatusCode())
 	})
 
+	t.Run("CreateWithoutOrg", func(t *testing.T) {
+		t.Parallel()
+		auditor := audit.NewMock()
+		client := coderdtest.New(t, &coderdtest.Options{Auditor: auditor})
+		numLogs := len(auditor.AuditLogs())
+
+		firstUser := coderdtest.CreateFirstUser(t, client)
+		numLogs++ // add an audit log for user create
+		numLogs++ // add an audit log for login
+
+		ctx, cancel := context.WithTimeout(context.Background(), testutil.WaitLong)
+		defer cancel()
+
+		user, err := client.CreateUser(ctx, codersdk.CreateUserRequest{
+			Email:    "another@user.org",
+			Username: "someone-else",
+			Password: "SomeSecurePassword!",
+		})
+		require.NoError(t, err)
+
+		require.Len(t, auditor.AuditLogs(), numLogs)
+		require.Equal(t, database.AuditActionCreate, auditor.AuditLogs()[numLogs-1].Action)
+		require.Equal(t, database.AuditActionLogin, auditor.AuditLogs()[numLogs-2].Action)
+
+		require.Len(t, user.OrganizationIDs, 1)
+		assert.Equal(t, firstUser.OrganizationID, user.OrganizationIDs[0])
+	})
+
 	t.Run("Create", func(t *testing.T) {
 		t.Parallel()
 		auditor := audit.NewMock()
 		client := coderdtest.New(t, &coderdtest.Options{Auditor: auditor})
 		numLogs := len(auditor.AuditLogs())
 
-		user := coderdtest.CreateFirstUser(t, client)
+		firstUser := coderdtest.CreateFirstUser(t, client)
 		numLogs++ // add an audit log for user create
 		numLogs++ // add an audit log for login
 
 		ctx, cancel := context.WithTimeout(context.Background(), testutil.WaitLong)
 		defer cancel()
 
-		_, err := client.CreateUser(ctx, codersdk.CreateUserRequest{
-			OrganizationID: user.OrganizationID,
+		user, err := client.CreateUser(ctx, codersdk.CreateUserRequest{
+			OrganizationID: firstUser.OrganizationID,
 			Email:          "another@user.org",
 			Username:       "someone-else",
 			Password:       "SomeSecurePassword!",
@@ -502,6 +531,9 @@ func TestPostUsers(t *testing.T) {
 		require.Len(t, auditor.AuditLogs(), numLogs)
 		require.Equal(t, database.AuditActionCreate, auditor.AuditLogs()[numLogs-1].Action)
 		require.Equal(t, database.AuditActionLogin, auditor.AuditLogs()[numLogs-2].Action)
+
+		require.Len(t, user.OrganizationIDs, 1)
+		assert.Equal(t, firstUser.OrganizationID, user.OrganizationIDs[0])
 	})
 
 	t.Run("LastSeenAt", func(t *testing.T) {
diff --git a/codersdk/users.go b/codersdk/users.go
index b0cebc720f665..157d3ef03cc5e 100644
--- a/codersdk/users.go
+++ b/codersdk/users.go
@@ -69,7 +69,7 @@ type CreateUserRequest struct {
 	Email          string    `json:"email" validate:"required,email" format:"email"`
 	Username       string    `json:"username" validate:"required,username"`
 	Password       string    `json:"password" validate:"required"`
-	OrganizationID uuid.UUID `json:"organization_id" validate:"required" format:"uuid"`
+	OrganizationID uuid.UUID `json:"organization_id" validate:"" format:"uuid"`
 }
 
 type UpdateUserProfileRequest struct {
diff --git a/docs/api/schemas.md b/docs/api/schemas.md
index 307b83544a449..6d527ee8d2d09 100644
--- a/docs/api/schemas.md
+++ b/docs/api/schemas.md
@@ -1564,7 +1564,7 @@ CreateParameterRequest is a structure used to create a new parameter value for a
 | Name              | Type   | Required | Restrictions | Description |
 | ----------------- | ------ | -------- | ------------ | ----------- |
 | `email`           | string | true     |              |             |
-| `organization_id` | string | true     |              |             |
+| `organization_id` | string | false    |              |             |
 | `password`        | string | true     |              |             |
 | `username`        | string | true     |              |             |
 
diff --git a/enterprise/coderd/scim.go b/enterprise/coderd/scim.go
index 9861c2217520d..8091bb4fe95eb 100644
--- a/enterprise/coderd/scim.go
+++ b/enterprise/coderd/scim.go
@@ -156,11 +156,27 @@ func (api *API) scimPostUser(rw http.ResponseWriter, r *http.Request) {
 		return
 	}
 
+	var organizationID uuid.UUID
+	//nolint:gocritic
+	organizations, err := api.Database.GetOrganizations(dbauthz.AsSystemRestricted(ctx))
+	if err != nil {
+		_ = handlerutil.WriteError(rw, err)
+		return
+	}
+
+	if len(organizations) > 0 {
+		// Add the user to the first organization. Once multi-organization
+		// support is added, we should enable a configuration map of user
+		// email to organization.
+		organizationID = organizations[0].ID
+	}
+
 	//nolint:gocritic // needed for SCIM
 	user, _, err := api.AGPL.CreateUser(dbauthz.AsSystemRestricted(ctx), api.Database, agpl.CreateUserRequest{
 		CreateUserRequest: codersdk.CreateUserRequest{
-			Username: sUser.UserName,
-			Email:    email,
+			Username:       sUser.UserName,
+			Email:          email,
+			OrganizationID: organizationID,
 		},
 		LoginType: database.LoginTypeOIDC,
 	})