diff --git a/cli/logout.go b/cli/logout.go
index 15d57b37c0f5b..90b7f8f3d653c 100644
--- a/cli/logout.go
+++ b/cli/logout.go
@@ -3,6 +3,7 @@ package cli
 import (
 	"fmt"
 	"os"
+	"strings"
 
 	"github.com/spf13/cobra"
 	"golang.org/x/xerrors"
@@ -15,11 +16,16 @@ func logout() *cobra.Command {
 		Use:   "logout",
 		Short: "Remove the local authenticated session",
 		RunE: func(cmd *cobra.Command, args []string) error {
-			var isLoggedOut bool
+			client, err := createClient(cmd)
+			if err != nil {
+				return err
+			}
+
+			var errors []error
 
 			config := createConfig(cmd)
 
-			_, err := cliui.Prompt(cmd, cliui.PromptOptions{
+			_, err = cliui.Prompt(cmd, cliui.PromptOptions{
 				Text:      "Are you sure you want to logout?",
 				IsConfirm: true,
 				Default:   "yes",
@@ -28,38 +34,40 @@ func logout() *cobra.Command {
 				return err
 			}
 
-			err = config.URL().Delete()
+			err = client.Logout(cmd.Context())
 			if err != nil {
-				// Only throw error if the URL configuration file is present,
-				// otherwise the user is already logged out, and we proceed
-				if !os.IsNotExist(err) {
-					return xerrors.Errorf("remove URL file: %w", err)
-				}
-				isLoggedOut = true
+				errors = append(errors, xerrors.Errorf("logout api: %w", err))
+			}
+
+			err = config.URL().Delete()
+			// Only throw error if the URL configuration file is present,
+			// otherwise the user is already logged out, and we proceed
+			if err != nil && !os.IsNotExist(err) {
+				errors = append(errors, xerrors.Errorf("remove URL file: %w", err))
 			}
 
 			err = config.Session().Delete()
-			if err != nil {
-				// Only throw error if the session configuration file is present,
-				// otherwise the user is already logged out, and we proceed
-				if !os.IsNotExist(err) {
-					return xerrors.Errorf("remove session file: %w", err)
-				}
-				isLoggedOut = true
+			// Only throw error if the session configuration file is present,
+			// otherwise the user is already logged out, and we proceed
+			if err != nil && !os.IsNotExist(err) {
+				errors = append(errors, xerrors.Errorf("remove session file: %w", err))
 			}
 
 			err = config.Organization().Delete()
 			// If the organization configuration file is absent, we still proceed
 			if err != nil && !os.IsNotExist(err) {
-				return xerrors.Errorf("remove organization file: %w", err)
+				errors = append(errors, xerrors.Errorf("remove organization file: %w", err))
 			}
 
-			// If the user was already logged out, we show them a different message
-			if isLoggedOut {
-				_, _ = fmt.Fprintf(cmd.OutOrStdout(), notLoggedInMessage+"\n")
-			} else {
-				_, _ = fmt.Fprintf(cmd.OutOrStdout(), caret+"Successfully logged out.\n")
+			if len(errors) > 0 {
+				var errorStringBuilder strings.Builder
+				for _, err := range errors {
+					_, _ = fmt.Fprint(&errorStringBuilder, "\t"+err.Error()+"\n")
+				}
+				errorString := strings.TrimRight(errorStringBuilder.String(), "\n")
+				return xerrors.New("Failed to log out.\n" + errorString)
 			}
+			_, _ = fmt.Fprintf(cmd.OutOrStdout(), caret+"You are no longer logged in. You can log in using 'coder login <url>'.\n")
 			return nil
 		},
 	}
diff --git a/cli/logout_test.go b/cli/logout_test.go
index bae15ef204ca4..753dcba234bfe 100644
--- a/cli/logout_test.go
+++ b/cli/logout_test.go
@@ -1,7 +1,10 @@
 package cli_test
 
 import (
+	"fmt"
 	"os"
+	"regexp"
+	"runtime"
 	"testing"
 
 	"github.com/stretchr/testify/assert"
@@ -21,7 +24,7 @@ func TestLogout(t *testing.T) {
 		pty := ptytest.New(t)
 		config := login(t, pty)
 
-		// ensure session files exist
+		// Ensure session files exist.
 		require.FileExists(t, string(config.URL()))
 		require.FileExists(t, string(config.Session()))
 
@@ -40,7 +43,7 @@ func TestLogout(t *testing.T) {
 
 		pty.ExpectMatch("Are you sure you want to logout?")
 		pty.WriteLine("yes")
-		pty.ExpectMatch("Successfully logged out")
+		pty.ExpectMatch("You are no longer logged in. You can log in using 'coder login <url>'.")
 		<-logoutChan
 	})
 	t.Run("SkipPrompt", func(t *testing.T) {
@@ -49,7 +52,7 @@ func TestLogout(t *testing.T) {
 		pty := ptytest.New(t)
 		config := login(t, pty)
 
-		// ensure session files exist
+		// Ensure session files exist.
 		require.FileExists(t, string(config.URL()))
 		require.FileExists(t, string(config.Session()))
 
@@ -66,7 +69,7 @@ func TestLogout(t *testing.T) {
 			assert.NoFileExists(t, string(config.Session()))
 		}()
 
-		pty.ExpectMatch("Successfully logged out")
+		pty.ExpectMatch("You are no longer logged in. You can log in using 'coder login <url>'.")
 		<-logoutChan
 	})
 	t.Run("NoURLFile", func(t *testing.T) {
@@ -75,7 +78,7 @@ func TestLogout(t *testing.T) {
 		pty := ptytest.New(t)
 		config := login(t, pty)
 
-		// ensure session files exist
+		// Ensure session files exist.
 		require.FileExists(t, string(config.URL()))
 		require.FileExists(t, string(config.Session()))
 
@@ -91,14 +94,9 @@ func TestLogout(t *testing.T) {
 		go func() {
 			defer close(logoutChan)
 			err := logout.Execute()
-			assert.NoError(t, err)
-			assert.NoFileExists(t, string(config.URL()))
-			assert.NoFileExists(t, string(config.Session()))
+			assert.EqualError(t, err, "You are not logged in. Try logging in using 'coder login <url>'.")
 		}()
 
-		pty.ExpectMatch("Are you sure you want to logout?")
-		pty.WriteLine("yes")
-		pty.ExpectMatch("You are not logged in. Try logging in using 'coder login <url>'.")
 		<-logoutChan
 	})
 	t.Run("NoSessionFile", func(t *testing.T) {
@@ -107,7 +105,7 @@ func TestLogout(t *testing.T) {
 		pty := ptytest.New(t)
 		config := login(t, pty)
 
-		// ensure session files exist
+		// Ensure session files exist.
 		require.FileExists(t, string(config.URL()))
 		require.FileExists(t, string(config.Session()))
 
@@ -123,14 +121,73 @@ func TestLogout(t *testing.T) {
 		go func() {
 			defer close(logoutChan)
 			err = logout.Execute()
-			assert.NoError(t, err)
-			assert.NoFileExists(t, string(config.URL()))
-			assert.NoFileExists(t, string(config.Session()))
+			assert.EqualError(t, err, "You are not logged in. Try logging in using 'coder login <url>'.")
+		}()
+
+		<-logoutChan
+	})
+	t.Run("CannotDeleteFiles", func(t *testing.T) {
+		t.Parallel()
+
+		pty := ptytest.New(t)
+		config := login(t, pty)
+
+		// Ensure session files exist.
+		require.FileExists(t, string(config.URL()))
+		require.FileExists(t, string(config.Session()))
+
+		var (
+			err         error
+			urlFile     *os.File
+			sessionFile *os.File
+		)
+		if runtime.GOOS == "windows" {
+			// Opening the files so Windows does not allow deleting them.
+			urlFile, err = os.Open(string(config.URL()))
+			require.NoError(t, err)
+			sessionFile, err = os.Open(string(config.Session()))
+			require.NoError(t, err)
+		} else {
+			// Changing the permissions to throw error during deletion.
+			err = os.Chmod(string(config), 0500)
+			require.NoError(t, err)
+		}
+		t.Cleanup(func() {
+			if runtime.GOOS == "windows" {
+				// Closing the opened files for cleanup.
+				err = urlFile.Close()
+				require.NoError(t, err)
+				err = sessionFile.Close()
+				require.NoError(t, err)
+			} else {
+				// Setting the permissions back for cleanup.
+				err = os.Chmod(string(config), 0700)
+				require.NoError(t, err)
+			}
+		})
+
+		logoutChan := make(chan struct{})
+		logout, _ := clitest.New(t, "logout", "--global-config", string(config))
+
+		logout.SetIn(pty.Input())
+		logout.SetOut(pty.Output())
+
+		go func() {
+			defer close(logoutChan)
+			err := logout.Execute()
+			assert.NotNil(t, err)
+			var errorMessage string
+			if runtime.GOOS == "windows" {
+				errorMessage = "The process cannot access the file because it is being used by another process."
+			} else {
+				errorMessage = "permission denied"
+			}
+			errRegex := regexp.MustCompile(fmt.Sprintf("Failed to log out.\n\tremove URL file: .+: %s\n\tremove session file: .+: %s", errorMessage, errorMessage))
+			assert.Regexp(t, errRegex, err.Error())
 		}()
 
 		pty.ExpectMatch("Are you sure you want to logout?")
 		pty.WriteLine("yes")
-		pty.ExpectMatch("You are not logged in. Try logging in using 'coder login <url>'.")
 		<-logoutChan
 	})
 }
diff --git a/coderd/coderd.go b/coderd/coderd.go
index c8c292a8a35b1..4513b2c86360a 100644
--- a/coderd/coderd.go
+++ b/coderd/coderd.go
@@ -219,7 +219,6 @@ func New(options *Options) *API {
 			r.Get("/first", api.firstUser)
 			r.Post("/first", api.postFirstUser)
 			r.Post("/login", api.postLogin)
-			r.Post("/logout", api.postLogout)
 			r.Get("/authmethods", api.userAuthMethods)
 			r.Route("/oauth2", func(r chi.Router) {
 				r.Route("/github", func(r chi.Router) {
@@ -234,6 +233,7 @@ func New(options *Options) *API {
 				)
 				r.Post("/", api.postUser)
 				r.Get("/", api.users)
+				r.Post("/logout", api.postLogout)
 				// These routes query information about site wide roles.
 				r.Route("/roles", func(r chi.Router) {
 					r.Get("/", api.assignableSiteRoles)
diff --git a/coderd/coderd_test.go b/coderd/coderd_test.go
index 4ca374ef7ed6a..d0aabb7a74758 100644
--- a/coderd/coderd_test.go
+++ b/coderd/coderd_test.go
@@ -104,6 +104,10 @@ func TestAuthorizeAllEndpoints(t *testing.T) {
 	workspaceRBACObj := rbac.ResourceWorkspace.InOrg(organization.ID).WithID(workspace.ID.String()).WithOwner(workspace.OwnerID.String())
 
 	// skipRoutes allows skipping routes from being checked.
+	skipRoutes := map[string]string{
+		"POST:/api/v2/users/logout": "Logging out deletes the API Key for other routes",
+	}
+
 	type routeCheck struct {
 		NoAuthorize  bool
 		AssertAction rbac.Action
@@ -117,7 +121,6 @@ func TestAuthorizeAllEndpoints(t *testing.T) {
 		"GET:/api/v2/users/first":       {NoAuthorize: true},
 		"POST:/api/v2/users/first":      {NoAuthorize: true},
 		"POST:/api/v2/users/login":      {NoAuthorize: true},
-		"POST:/api/v2/users/logout":     {NoAuthorize: true},
 		"GET:/api/v2/users/authmethods": {NoAuthorize: true},
 		"POST:/api/v2/csp/reports":      {NoAuthorize: true},
 
@@ -310,8 +313,20 @@ func TestAuthorizeAllEndpoints(t *testing.T) {
 		assertRoute[noTrailSlash] = v
 	}
 
+	for k, v := range skipRoutes {
+		noTrailSlash := strings.TrimRight(k, "/")
+		if _, ok := skipRoutes[noTrailSlash]; ok && noTrailSlash != k {
+			t.Errorf("route %q & %q is declared twice", noTrailSlash, k)
+			t.FailNow()
+		}
+		skipRoutes[noTrailSlash] = v
+	}
+
 	err = chi.Walk(api.Handler, func(method string, route string, handler http.Handler, middlewares ...func(http.Handler) http.Handler) error {
 		name := method + ":" + route
+		if _, ok := skipRoutes[strings.TrimRight(name, "/")]; ok {
+			return nil
+		}
 		t.Run(name, func(t *testing.T) {
 			authorizer.reset()
 			routeAssertions, ok := assertRoute[strings.TrimRight(name, "/")]
diff --git a/coderd/database/databasefake/databasefake.go b/coderd/database/databasefake/databasefake.go
index 6acc5d156bdac..8d9edc6f02523 100644
--- a/coderd/database/databasefake/databasefake.go
+++ b/coderd/database/databasefake/databasefake.go
@@ -126,6 +126,21 @@ func (q *fakeQuerier) GetAPIKeyByID(_ context.Context, id string) (database.APIK
 	return database.APIKey{}, sql.ErrNoRows
 }
 
+func (q *fakeQuerier) DeleteAPIKeyByID(_ context.Context, id string) error {
+	q.mutex.Lock()
+	defer q.mutex.Unlock()
+
+	for index, apiKey := range q.apiKeys {
+		if apiKey.ID != id {
+			continue
+		}
+		q.apiKeys[index] = q.apiKeys[len(q.apiKeys)-1]
+		q.apiKeys = q.apiKeys[:len(q.apiKeys)-1]
+		return nil
+	}
+	return sql.ErrNoRows
+}
+
 func (q *fakeQuerier) GetFileByHash(_ context.Context, hash string) (database.File, error) {
 	q.mutex.RLock()
 	defer q.mutex.RUnlock()
diff --git a/coderd/database/querier.go b/coderd/database/querier.go
index db061cfcb36a1..7d4c361cea05b 100644
--- a/coderd/database/querier.go
+++ b/coderd/database/querier.go
@@ -18,6 +18,7 @@ type querier interface {
 	// multiple provisioners from acquiring the same jobs. See:
 	// https://www.postgresql.org/docs/9.5/sql-select.html#SQL-FOR-UPDATE-SHARE
 	AcquireProvisionerJob(ctx context.Context, arg AcquireProvisionerJobParams) (ProvisionerJob, error)
+	DeleteAPIKeyByID(ctx context.Context, id string) error
 	DeleteGitSSHKey(ctx context.Context, userID uuid.UUID) error
 	DeleteParameterValueByID(ctx context.Context, id uuid.UUID) error
 	GetAPIKeyByID(ctx context.Context, id string) (APIKey, error)
diff --git a/coderd/database/queries.sql.go b/coderd/database/queries.sql.go
index 137fe36b4456b..8724fbbc8e474 100644
--- a/coderd/database/queries.sql.go
+++ b/coderd/database/queries.sql.go
@@ -15,6 +15,19 @@ import (
 	"github.com/tabbed/pqtype"
 )
 
+const deleteAPIKeyByID = `-- name: DeleteAPIKeyByID :exec
+DELETE
+FROM
+	api_keys
+WHERE
+	id = $1
+`
+
+func (q *sqlQuerier) DeleteAPIKeyByID(ctx context.Context, id string) error {
+	_, err := q.db.ExecContext(ctx, deleteAPIKeyByID, id)
+	return err
+}
+
 const getAPIKeyByID = `-- name: GetAPIKeyByID :one
 SELECT
 	id, hashed_secret, user_id, last_used, expires_at, created_at, updated_at, login_type, oauth_access_token, oauth_refresh_token, oauth_id_token, oauth_expiry
diff --git a/coderd/database/queries/apikeys.sql b/coderd/database/queries/apikeys.sql
index 1af2016f491bf..38ac145ce465e 100644
--- a/coderd/database/queries/apikeys.sql
+++ b/coderd/database/queries/apikeys.sql
@@ -38,3 +38,10 @@ SET
 	oauth_expiry = $6
 WHERE
 	id = $1;
+
+-- name: DeleteAPIKeyByID :exec
+DELETE
+FROM
+	api_keys
+WHERE
+	id = $1;
diff --git a/coderd/users.go b/coderd/users.go
index 02d46655d4f54..f4b87e6a98ebc 100644
--- a/coderd/users.go
+++ b/coderd/users.go
@@ -85,7 +85,7 @@ func (api *API) postFirstUser(rw http.ResponseWriter, r *http.Request) {
 	// TODO: @emyrk this currently happens outside the database tx used to create
 	// 	the user. Maybe I add this ability to grant roles in the createUser api
 	//	and add some rbac bypass when calling api functions this way??
-	// Add the admin role to this first user
+	// Add the admin role to this first user.
 	_, err = api.Database.UpdateUserRoles(r.Context(), database.UpdateUserRolesParams{
 		GrantedRoles: []string{rbac.RoleAdmin(), rbac.RoleMember()},
 		ID:           user.ID,
@@ -109,7 +109,7 @@ func (api *API) users(rw http.ResponseWriter, r *http.Request) {
 		statusFilter = r.URL.Query().Get("status")
 	)
 
-	// Reading all users across the site
+	// Reading all users across the site.
 	if !api.Authorize(rw, r, rbac.ActionRead, rbac.ResourceUser) {
 		return
 	}
@@ -162,7 +162,7 @@ func (api *API) users(rw http.ResponseWriter, r *http.Request) {
 
 // Creates a new user.
 func (api *API) postUser(rw http.ResponseWriter, r *http.Request) {
-	// Create the user on the site
+	// Create the user on the site.
 	if !api.Authorize(rw, r, rbac.ActionCreate, rbac.ResourceUser) {
 		return
 	}
@@ -408,11 +408,11 @@ func (api *API) userRoles(rw http.ResponseWriter, r *http.Request) {
 		return
 	}
 
-	// Only include ones we can read from RBAC
+	// Only include ones we can read from RBAC.
 	memberships = AuthorizeFilter(api, r, rbac.ActionRead, memberships)
 
 	for _, mem := range memberships {
-		// If we can read the org member, include the roles
+		// If we can read the org member, include the roles.
 		if err == nil {
 			resp.OrganizationRoles[mem.OrganizationID] = mem.Roles
 		}
@@ -422,7 +422,7 @@ func (api *API) userRoles(rw http.ResponseWriter, r *http.Request) {
 }
 
 func (api *API) putUserRoles(rw http.ResponseWriter, r *http.Request) {
-	// User is the user to modify
+	// User is the user to modify.
 	user := httpmw.UserParam(r)
 	roles := httpmw.UserRoles(r)
 
@@ -470,7 +470,7 @@ func (api *API) putUserRoles(rw http.ResponseWriter, r *http.Request) {
 // updateSiteUserRoles will ensure only site wide roles are passed in as arguments.
 // If an organization role is included, an error is returned.
 func (api *API) updateSiteUserRoles(ctx context.Context, args database.UpdateUserRolesParams) (database.User, error) {
-	// Enforce only site wide roles
+	// Enforce only site wide roles.
 	for _, r := range args.GrantedRoles {
 		if _, ok := rbac.IsOrgRole(r); ok {
 			return database.User{}, xerrors.Errorf("must only update site wide roles")
@@ -504,7 +504,7 @@ func (api *API) organizationsByUser(rw http.ResponseWriter, r *http.Request) {
 		return
 	}
 
-	// Only return orgs the user can read
+	// Only return orgs the user can read.
 	organizations = AuthorizeFilter(api, r, rbac.ActionRead, organizations)
 
 	publicOrganizations := make([]codersdk.Organization, 0, len(organizations))
@@ -585,7 +585,7 @@ func (api *API) postLogin(rw http.ResponseWriter, r *http.Request) {
 	})
 }
 
-// Creates a new session key, used for logging in via the CLI
+// Creates a new session key, used for logging in via the CLI.
 func (api *API) postAPIKey(rw http.ResponseWriter, r *http.Request) {
 	user := httpmw.UserParam(r)
 
@@ -604,17 +604,28 @@ func (api *API) postAPIKey(rw http.ResponseWriter, r *http.Request) {
 	httpapi.Write(rw, http.StatusCreated, codersdk.GenerateAPIKeyResponse{Key: sessionToken})
 }
 
-// Clear the user's session cookie
-func (*API) postLogout(rw http.ResponseWriter, _ *http.Request) {
-	// Get a blank token cookie
+// Clear the user's session cookie.
+func (api *API) postLogout(rw http.ResponseWriter, r *http.Request) {
+	// Get a blank token cookie.
 	cookie := &http.Cookie{
-		// MaxAge < 0 means to delete the cookie now
+		// MaxAge < 0 means to delete the cookie now.
 		MaxAge: -1,
 		Name:   httpmw.SessionTokenKey,
 		Path:   "/",
 	}
 
 	http.SetCookie(rw, cookie)
+
+	// Delete the session token from database.
+	apiKey := httpmw.APIKey(r)
+	err := api.Database.DeleteAPIKeyByID(r.Context(), apiKey.ID)
+	if err != nil {
+		httpapi.Write(rw, http.StatusInternalServerError, httpapi.Response{
+			Message: fmt.Sprintf("delete api key: %s", err.Error()),
+		})
+		return
+	}
+
 	httpapi.Write(rw, http.StatusOK, httpapi.Response{
 		Message: "Logged out!",
 	})
@@ -696,7 +707,7 @@ func (api *API) createUser(ctx context.Context, req codersdk.CreateUserRequest)
 			req.OrganizationID = organization.ID
 			orgRoles = append(orgRoles, rbac.RoleOrgAdmin(req.OrganizationID))
 		}
-		// Always also be a member
+		// Always also be a member.
 		orgRoles = append(orgRoles, rbac.RoleOrgMember(req.OrganizationID))
 
 		params := database.InsertUserParams{
@@ -742,7 +753,7 @@ func (api *API) createUser(ctx context.Context, req codersdk.CreateUserRequest)
 			UserID:         user.ID,
 			CreatedAt:      database.Now(),
 			UpdatedAt:      database.Now(),
-			// By default give them membership to the organization
+			// By default give them membership to the organization.
 			Roles: orgRoles,
 		})
 		if err != nil {
diff --git a/coderd/users_test.go b/coderd/users_test.go
index d8d05542df092..0c31d5c9259aa 100644
--- a/coderd/users_test.go
+++ b/coderd/users_test.go
@@ -2,15 +2,18 @@ package coderd_test
 
 import (
 	"context"
+	"database/sql"
 	"fmt"
 	"net/http"
 	"sort"
+	"strings"
 	"testing"
 
 	"github.com/google/uuid"
 	"github.com/stretchr/testify/require"
 
 	"github.com/coder/coder/coderd/coderdtest"
+	"github.com/coder/coder/coderd/database/databasefake"
 	"github.com/coder/coder/coderd/httpmw"
 	"github.com/coder/coder/coderd/rbac"
 	"github.com/coder/coder/codersdk"
@@ -103,27 +106,71 @@ func TestPostLogin(t *testing.T) {
 func TestPostLogout(t *testing.T) {
 	t.Parallel()
 
-	t.Run("ClearCookie", func(t *testing.T) {
+	// Checks that the cookie is cleared and the API Key is deleted from the database.
+	t.Run("Logout", func(t *testing.T) {
 		t.Parallel()
 
-		client := coderdtest.New(t, nil)
+		ctx := context.Background()
+		client, api := coderdtest.NewWithAPI(t, nil)
+		_ = coderdtest.CreateFirstUser(t, client)
+		keyID := strings.Split(client.SessionToken, "-")[0]
+
+		apiKey, err := api.Database.GetAPIKeyByID(ctx, keyID)
+		require.NoError(t, err)
+		require.Equal(t, keyID, apiKey.ID, "API key should exist in the database")
+
 		fullURL, err := client.URL.Parse("/api/v2/users/logout")
 		require.NoError(t, err, "Server URL should parse successfully")
 
-		req, err := http.NewRequestWithContext(context.Background(), http.MethodPost, fullURL.String(), nil)
-		require.NoError(t, err, "/logout request construction should succeed")
+		res, err := client.Request(ctx, http.MethodPost, fullURL.String(), nil)
+		require.NoError(t, err, "/logout request should succeed")
+		res.Body.Close()
+		require.Equal(t, http.StatusOK, res.StatusCode)
+
+		cookies := res.Cookies()
+		require.Len(t, cookies, 1, "Exactly one cookie should be returned")
 
-		httpClient := &http.Client{}
+		require.Equal(t, httpmw.SessionTokenKey, cookies[0].Name, "Cookie should be the auth cookie")
+		require.Equal(t, -1, cookies[0].MaxAge, "Cookie should be set to delete")
 
-		response, err := httpClient.Do(req)
+		apiKey, err = api.Database.GetAPIKeyByID(ctx, keyID)
+		require.ErrorIs(t, err, sql.ErrNoRows, "API key should not exist in the database")
+	})
+
+	t.Run("LogoutWithoutKey", func(t *testing.T) {
+		t.Parallel()
+
+		ctx := context.Background()
+		client, api := coderdtest.NewWithAPI(t, nil)
+		_ = coderdtest.CreateFirstUser(t, client)
+		keyID := strings.Split(client.SessionToken, "-")[0]
+
+		apiKey, err := api.Database.GetAPIKeyByID(ctx, keyID)
+		require.NoError(t, err)
+		require.Equal(t, keyID, apiKey.ID, "API key should exist in the database")
+
+		// Setting a fake database without the API Key to be used by the API.
+		// The middleware that extracts the API key is already set to read
+		// from the original database.
+		dbWithoutKey := databasefake.New()
+		api.Database = dbWithoutKey
+
+		fullURL, err := client.URL.Parse("/api/v2/users/logout")
+		require.NoError(t, err, "Server URL should parse successfully")
+
+		res, err := client.Request(ctx, http.MethodPost, fullURL.String(), nil)
 		require.NoError(t, err, "/logout request should succeed")
-		response.Body.Close()
+		res.Body.Close()
+		require.Equal(t, http.StatusInternalServerError, res.StatusCode)
 
-		cookies := response.Cookies()
+		cookies := res.Cookies()
 		require.Len(t, cookies, 1, "Exactly one cookie should be returned")
 
-		require.Equal(t, cookies[0].Name, httpmw.SessionTokenKey, "Cookie should be the auth cookie")
-		require.Equal(t, cookies[0].MaxAge, -1, "Cookie should be set to delete")
+		require.Equal(t, httpmw.SessionTokenKey, cookies[0].Name, "Cookie should be the auth cookie")
+		require.Equal(t, -1, cookies[0].MaxAge, "Cookie should be set to delete")
+
+		apiKey, err = api.Database.GetAPIKeyByID(ctx, keyID)
+		require.ErrorIs(t, err, sql.ErrNoRows, "API key should not exist in the database")
 	})
 }