diff --git a/cli/login.go b/cli/login.go
index 5910b5846ddcd..9658edb835c2e 100644
--- a/cli/login.go
+++ b/cli/login.go
@@ -2,13 +2,17 @@ package cli
 
 import (
 	"fmt"
+	"io/ioutil"
 	"net/url"
+	"os/exec"
 	"os/user"
+	"runtime"
 	"strings"
 
 	"github.com/fatih/color"
 	"github.com/go-playground/validator/v10"
 	"github.com/manifoldco/promptui"
+	"github.com/pkg/browser"
 	"github.com/spf13/cobra"
 	"golang.org/x/xerrors"
 
@@ -16,6 +20,21 @@ import (
 	"github.com/coder/coder/codersdk"
 )
 
+const (
+	goosWindows = "windows"
+	goosDarwin  = "darwin"
+)
+
+func init() {
+	// Hide output from the browser library,
+	// otherwise we can get really verbose and non-actionable messages
+	// when in SSH or another type of headless session
+	// NOTE: This needs to be in `init` to prevent data races
+	// (multiple threads trying to set the global browser.Std* variables)
+	browser.Stderr = ioutil.Discard
+	browser.Stdout = ioutil.Discard
+}
+
 func login() *cobra.Command {
 	return &cobra.Command{
 		Use:  "login <url>",
@@ -116,8 +135,10 @@ func login() *cobra.Command {
 				if err != nil {
 					return xerrors.Errorf("login with password: %w", err)
 				}
+
+				sessionToken := resp.SessionToken
 				config := createConfig(cmd)
-				err = config.Session().Write(resp.SessionToken)
+				err = config.Session().Write(sessionToken)
 				if err != nil {
 					return xerrors.Errorf("write session token: %w", err)
 				}
@@ -130,7 +151,82 @@ func login() *cobra.Command {
 				return nil
 			}
 
+			authURL := *serverURL
+			authURL.Path = serverURL.Path + "/cli-auth"
+			if err := openURL(authURL.String()); err != nil {
+				_, _ = fmt.Fprintf(cmd.OutOrStdout(), "Open the following in your browser:\n\n\t%s\n\n", authURL.String())
+			} else {
+				_, _ = fmt.Fprintf(cmd.OutOrStdout(), "Your browser has been opened to visit:\n\n\t%s\n\n", authURL.String())
+			}
+
+			sessionToken, err := prompt(cmd, &promptui.Prompt{
+				Label: "Paste your token here:",
+				Mask:  '*',
+				Validate: func(token string) error {
+					client.SessionToken = token
+					_, err := client.User(cmd.Context(), "me")
+					if err != nil {
+						return xerrors.New("That's not a valid token!")
+					}
+					return err
+				},
+			})
+			if err != nil {
+				return xerrors.Errorf("paste token prompt: %w", err)
+			}
+
+			// Login to get user data - verify it is OK before persisting
+			client.SessionToken = sessionToken
+			resp, err := client.User(cmd.Context(), "me")
+			if err != nil {
+				return xerrors.Errorf("get user: %w", err)
+			}
+
+			config := createConfig(cmd)
+			err = config.Session().Write(sessionToken)
+			if err != nil {
+				return xerrors.Errorf("write session token: %w", err)
+			}
+			err = config.URL().Write(serverURL.String())
+			if err != nil {
+				return xerrors.Errorf("write server url: %w", err)
+			}
+
+			_, _ = fmt.Fprintf(cmd.OutOrStdout(), "%s Welcome to Coder, %s! You're authenticated.\n", color.HiBlackString(">"), color.HiCyanString(resp.Username))
 			return nil
 		},
 	}
 }
+
+// isWSL determines if coder-cli is running within Windows Subsystem for Linux
+func isWSL() (bool, error) {
+	if runtime.GOOS == goosDarwin || runtime.GOOS == goosWindows {
+		return false, nil
+	}
+	data, err := ioutil.ReadFile("/proc/version")
+	if err != nil {
+		return false, xerrors.Errorf("read /proc/version: %w", err)
+	}
+	return strings.Contains(strings.ToLower(string(data)), "microsoft"), nil
+}
+
+// openURL opens the provided URL via user's default browser
+func openURL(urlToOpen string) error {
+	var cmd string
+	var args []string
+
+	wsl, err := isWSL()
+	if err != nil {
+		return xerrors.Errorf("test running Windows Subsystem for Linux: %w", err)
+	}
+
+	if wsl {
+		cmd = "cmd.exe"
+		args = []string{"/c", "start"}
+		urlToOpen = strings.ReplaceAll(urlToOpen, "&", "^&")
+		args = append(args, urlToOpen)
+		return exec.Command(cmd, args...).Start()
+	}
+
+	return browser.OpenURL(urlToOpen)
+}
diff --git a/cli/login_test.go b/cli/login_test.go
index 24caf18e1aa3f..e9f3cc13ecf3f 100644
--- a/cli/login_test.go
+++ b/cli/login_test.go
@@ -1,11 +1,13 @@
 package cli_test
 
 import (
+	"context"
 	"testing"
 
 	"github.com/stretchr/testify/require"
 
 	"github.com/coder/coder/cli/clitest"
+	"github.com/coder/coder/coderd"
 	"github.com/coder/coder/coderd/coderdtest"
 	"github.com/coder/coder/pty/ptytest"
 )
@@ -50,4 +52,60 @@ func TestLogin(t *testing.T) {
 		}
 		pty.ExpectMatch("Welcome to Coder")
 	})
+
+	t.Run("ExistingUserValidTokenTTY", func(t *testing.T) {
+		t.Parallel()
+		client := coderdtest.New(t)
+		_, err := client.CreateInitialUser(context.Background(), coderd.CreateInitialUserRequest{
+			Username:     "test-user",
+			Email:        "test-user@coder.com",
+			Organization: "acme-corp",
+			Password:     "password",
+		})
+		require.NoError(t, err)
+		token, err := client.LoginWithPassword(context.Background(), coderd.LoginWithPasswordRequest{
+			Email:    "test-user@coder.com",
+			Password: "password",
+		})
+		require.NoError(t, err)
+
+		root, _ := clitest.New(t, "login", client.URL.String(), "--force-tty")
+		pty := ptytest.New(t)
+		root.SetIn(pty.Input())
+		root.SetOut(pty.Output())
+		go func() {
+			err := root.Execute()
+			require.NoError(t, err)
+		}()
+
+		pty.ExpectMatch("Paste your token here:")
+		pty.WriteLine(token.SessionToken)
+		pty.ExpectMatch("Welcome to Coder")
+	})
+
+	t.Run("ExistingUserInvalidTokenTTY", func(t *testing.T) {
+		t.Parallel()
+		client := coderdtest.New(t)
+		_, err := client.CreateInitialUser(context.Background(), coderd.CreateInitialUserRequest{
+			Username:     "test-user",
+			Email:        "test-user@coder.com",
+			Organization: "acme-corp",
+			Password:     "password",
+		})
+		require.NoError(t, err)
+
+		root, _ := clitest.New(t, "login", client.URL.String(), "--force-tty")
+		pty := ptytest.New(t)
+		root.SetIn(pty.Input())
+		root.SetOut(pty.Output())
+		go func() {
+			err := root.Execute()
+			// An error is expected in this case, since the login wasn't successful:
+			require.Error(t, err)
+		}()
+
+		pty.ExpectMatch("Paste your token here:")
+		pty.WriteLine("an-invalid-token")
+		pty.ExpectMatch("That's not a valid token!")
+	})
 }
diff --git a/coderd/coderd.go b/coderd/coderd.go
index 9669dbf92c2e1..1213b04aa0a86 100644
--- a/coderd/coderd.go
+++ b/coderd/coderd.go
@@ -36,6 +36,7 @@ func New(options *Options) http.Handler {
 		})
 		r.Post("/login", api.postLogin)
 		r.Post("/logout", api.postLogout)
+
 		// Used for setup.
 		r.Get("/user", api.user)
 		r.Post("/user", api.postUser)
@@ -44,10 +45,12 @@ func New(options *Options) http.Handler {
 				httpmw.ExtractAPIKey(options.Database, nil),
 			)
 			r.Post("/", api.postUsers)
-			r.Group(func(r chi.Router) {
+
+			r.Route("/{user}", func(r chi.Router) {
 				r.Use(httpmw.ExtractUserParam(options.Database))
-				r.Get("/{user}", api.userByName)
-				r.Get("/{user}/organizations", api.organizationsByUser)
+				r.Get("/", api.userByName)
+				r.Get("/organizations", api.organizationsByUser)
+				r.Post("/keys", api.postKeyForUser)
 			})
 		})
 		r.Route("/projects", func(r chi.Router) {
diff --git a/coderd/users.go b/coderd/users.go
index ab6328fbe1984..a660f31fdfa94 100644
--- a/coderd/users.go
+++ b/coderd/users.go
@@ -55,6 +55,11 @@ type LoginWithPasswordResponse struct {
 	SessionToken string `json:"session_token" validate:"required"`
 }
 
+// GenerateAPIKeyResponse contains an API key for a user.
+type GenerateAPIKeyResponse struct {
+	Key string `json:"key"`
+}
+
 // Returns whether the initial user has been created or not.
 func (api *api) user(rw http.ResponseWriter, r *http.Request) {
 	userCount, err := api.Database.GetUserCount(r.Context())
@@ -312,6 +317,50 @@ func (api *api) postLogin(rw http.ResponseWriter, r *http.Request) {
 	})
 }
 
+// Creates a new session key, used for logging in via the CLI
+func (api *api) postKeyForUser(rw http.ResponseWriter, r *http.Request) {
+	user := httpmw.UserParam(r)
+	apiKey := httpmw.APIKey(r)
+
+	if user.ID != apiKey.UserID {
+		httpapi.Write(rw, http.StatusUnauthorized, httpapi.Response{
+			Message: "Keys can only be generated for the authenticated user",
+		})
+		return
+	}
+
+	keyID, keySecret, err := generateAPIKeyIDSecret()
+	if err != nil {
+		httpapi.Write(rw, http.StatusInternalServerError, httpapi.Response{
+			Message: fmt.Sprintf("generate api key parts: %s", err.Error()),
+		})
+		return
+	}
+	hashed := sha256.Sum256([]byte(keySecret))
+
+	_, err = api.Database.InsertAPIKey(r.Context(), database.InsertAPIKeyParams{
+		ID:           keyID,
+		UserID:       apiKey.UserID,
+		ExpiresAt:    database.Now().AddDate(1, 0, 0), // Expire after 1 year (same as v1)
+		CreatedAt:    database.Now(),
+		UpdatedAt:    database.Now(),
+		HashedSecret: hashed[:],
+		LoginType:    database.LoginTypeBuiltIn,
+	})
+	if err != nil {
+		httpapi.Write(rw, http.StatusInternalServerError, httpapi.Response{
+			Message: fmt.Sprintf("insert api key: %s", err.Error()),
+		})
+		return
+	}
+
+	// This format is consumed by the APIKey middleware.
+	generatedAPIKey := fmt.Sprintf("%s-%s", keyID, keySecret)
+
+	render.Status(r, http.StatusCreated)
+	render.JSON(rw, r, GenerateAPIKeyResponse{Key: generatedAPIKey})
+}
+
 // Clear the user's session cookie
 func (*api) postLogout(rw http.ResponseWriter, r *http.Request) {
 	// Get a blank token cookie
diff --git a/coderd/users_test.go b/coderd/users_test.go
index 8ef1464856f75..3a3a5ee8eac76 100644
--- a/coderd/users_test.go
+++ b/coderd/users_test.go
@@ -119,6 +119,33 @@ func TestOrganizationsByUser(t *testing.T) {
 	require.Len(t, orgs, 1)
 }
 
+func TestPostKey(t *testing.T) {
+	t.Parallel()
+	t.Run("InvalidUser", func(t *testing.T) {
+		t.Parallel()
+		client := coderdtest.New(t)
+		_ = coderdtest.CreateInitialUser(t, client)
+
+		// Clear session token
+		client.SessionToken = ""
+		// ...and request an API key
+		_, err := client.CreateAPIKey(context.Background())
+		var apiErr *codersdk.Error
+		require.ErrorAs(t, err, &apiErr)
+		require.Equal(t, http.StatusUnauthorized, apiErr.StatusCode())
+	})
+
+	t.Run("Success", func(t *testing.T) {
+		t.Parallel()
+		client := coderdtest.New(t)
+		_ = coderdtest.CreateInitialUser(t, client)
+		apiKey, err := client.CreateAPIKey(context.Background())
+		require.NotNil(t, apiKey)
+		require.GreaterOrEqual(t, len(apiKey.Key), 2)
+		require.NoError(t, err)
+	})
+}
+
 func TestPostLogin(t *testing.T) {
 	t.Parallel()
 	t.Run("InvalidUser", func(t *testing.T) {
diff --git a/codersdk/users.go b/codersdk/users.go
index b17b5a9931e6e..08b152f9cf8d0 100644
--- a/codersdk/users.go
+++ b/codersdk/users.go
@@ -56,6 +56,20 @@ func (c *Client) CreateUser(ctx context.Context, req coderd.CreateUserRequest) (
 	return user, json.NewDecoder(res.Body).Decode(&user)
 }
 
+// CreateAPIKey calls the /api-key API
+func (c *Client) CreateAPIKey(ctx context.Context) (*coderd.GenerateAPIKeyResponse, error) {
+	res, err := c.request(ctx, http.MethodPost, "/api/v2/users/me/keys", nil)
+	if err != nil {
+		return nil, err
+	}
+	defer res.Body.Close()
+	if res.StatusCode > http.StatusCreated {
+		return nil, readBodyAsError(res)
+	}
+	apiKey := &coderd.GenerateAPIKeyResponse{}
+	return apiKey, json.NewDecoder(res.Body).Decode(apiKey)
+}
+
 // LoginWithPassword creates a session token authenticating with an email and password.
 // Call `SetSessionToken()` to apply the newly acquired token to the client.
 func (c *Client) LoginWithPassword(ctx context.Context, req coderd.LoginWithPasswordRequest) (coderd.LoginWithPasswordResponse, error) {
diff --git a/go.mod b/go.mod
index e224d221c55bc..5c13f4423b4e4 100644
--- a/go.mod
+++ b/go.mod
@@ -115,6 +115,7 @@ require (
 	github.com/pion/stun v0.3.5 // indirect
 	github.com/pion/turn/v2 v2.0.6 // indirect
 	github.com/pion/udp v0.1.1 // indirect
+	github.com/pkg/browser v0.0.0-20210911075715-681adbf594b8 // indirect
 	github.com/pkg/errors v0.9.1 // indirect
 	github.com/pmezard/go-difflib v1.0.0 // indirect
 	github.com/sirupsen/logrus v1.8.1 // indirect
diff --git a/go.sum b/go.sum
index 416fe1da0f69d..049f05866af57 100644
--- a/go.sum
+++ b/go.sum
@@ -1062,6 +1062,7 @@ github.com/pion/udp v0.1.1/go.mod h1:6AFo+CMdKQm7UiA0eUPA8/eVCTx8jBIITLZHc9DWX5M
 github.com/pion/webrtc/v3 v3.1.23 h1:suyNiF9o2/6SBsyWA1UweraUWYkaHCNJdt/16b61I5w=
 github.com/pion/webrtc/v3 v3.1.23/go.mod h1:L5S/oAhL0Fzt/rnftVQRrP80/j5jygY7XRZzWwFx6P4=
 github.com/pkg/browser v0.0.0-20210706143420-7d21f8c997e2/go.mod h1:HKlIX3XHQyzLZPlr7++PzdhaXEj94dEiJgZDTsxEqUI=
+github.com/pkg/browser v0.0.0-20210911075715-681adbf594b8 h1:KoWmjvw+nsYOo29YJK9vDA65RGE3NrOnUtO7a+RF9HU=
 github.com/pkg/browser v0.0.0-20210911075715-681adbf594b8/go.mod h1:HKlIX3XHQyzLZPlr7++PzdhaXEj94dEiJgZDTsxEqUI=
 github.com/pkg/diff v0.0.0-20210226163009-20ebb0f2a09e/go.mod h1:pJLUxLENpZxwdsKMEsNbx1VGcRFpLqf3715MtcvvzbA=
 github.com/pkg/errors v0.8.0/go.mod h1:bwawxfHBFNV+L2hUp1rHADufV3IMtnDRdf1r5NINEl0=
diff --git a/site/api.ts b/site/api.ts
index 0a11659ed24d7..5339ccd15d851 100644
--- a/site/api.ts
+++ b/site/api.ts
@@ -139,3 +139,16 @@ export const logout = async (): Promise<void> => {
 
   return
 }
+
+export const getApiKey = async (): Promise<{ key: string }> => {
+  const response = await fetch("/api/v2/users/me/keys", {
+    method: "POST",
+  })
+
+  if (!response.ok) {
+    const body = await response.json()
+    throw new Error(body.message)
+  }
+
+  return await response.json()
+}
diff --git a/site/components/SignIn/CliAuthToken.stories.tsx b/site/components/SignIn/CliAuthToken.stories.tsx
new file mode 100644
index 0000000000000..b9d8e5baa9a47
--- /dev/null
+++ b/site/components/SignIn/CliAuthToken.stories.tsx
@@ -0,0 +1,16 @@
+import { Story } from "@storybook/react"
+import React from "react"
+import { CliAuthToken, CliAuthTokenProps } from "./CliAuthToken"
+
+export default {
+  title: "SignIn/CliAuthToken",
+  component: CliAuthToken,
+  argTypes: {
+    sessionToken: { control: "text", defaultValue: "some-session-token" },
+  },
+}
+
+const Template: Story<CliAuthTokenProps> = (args) => <CliAuthToken {...args} />
+
+export const Example = Template.bind({})
+Example.args = {}
diff --git a/site/components/SignIn/CliAuthToken.test.tsx b/site/components/SignIn/CliAuthToken.test.tsx
new file mode 100644
index 0000000000000..d17fdbcce88ea
--- /dev/null
+++ b/site/components/SignIn/CliAuthToken.test.tsx
@@ -0,0 +1,16 @@
+import React from "react"
+import { screen } from "@testing-library/react"
+import { render } from "../../test_helpers"
+
+import { CliAuthToken } from "./CliAuthToken"
+
+describe("CliAuthToken", () => {
+  it("renders content", async () => {
+    // When
+    render(<CliAuthToken sessionToken="test-token" />)
+
+    // Then
+    await screen.findByText("Session Token")
+    await screen.findByText("test-token")
+  })
+})
diff --git a/site/components/SignIn/CliAuthToken.tsx b/site/components/SignIn/CliAuthToken.tsx
new file mode 100644
index 0000000000000..a6d0886e60ebf
--- /dev/null
+++ b/site/components/SignIn/CliAuthToken.tsx
@@ -0,0 +1,29 @@
+import Paper from "@material-ui/core/Paper"
+import Typography from "@material-ui/core/Typography"
+import { makeStyles } from "@material-ui/core/styles"
+import React from "react"
+import { CodeExample } from "../CodeExample"
+
+export interface CliAuthTokenProps {
+  sessionToken: string
+}
+
+export const CliAuthToken: React.FC<CliAuthTokenProps> = ({ sessionToken }) => {
+  const styles = useStyles()
+  return (
+    <Paper className={styles.container}>
+      <Typography className={styles.title}>Session Token</Typography>
+      <CodeExample code={sessionToken} />
+    </Paper>
+  )
+}
+
+const useStyles = makeStyles((theme) => ({
+  title: {
+    marginBottom: theme.spacing(2),
+  },
+  container: {
+    maxWidth: "680px",
+    padding: theme.spacing(2),
+  },
+}))
diff --git a/site/components/SignIn/index.tsx b/site/components/SignIn/index.tsx
index 6ea6f3de7dd2a..066b58003c67c 100644
--- a/site/components/SignIn/index.tsx
+++ b/site/components/SignIn/index.tsx
@@ -1 +1,2 @@
+export * from "./CliAuthToken"
 export * from "./SignInForm"
diff --git a/site/pages/cli-auth.tsx b/site/pages/cli-auth.tsx
new file mode 100644
index 0000000000000..a31c682d93090
--- /dev/null
+++ b/site/pages/cli-auth.tsx
@@ -0,0 +1,44 @@
+import { makeStyles } from "@material-ui/core/styles"
+import React, { useEffect, useState } from "react"
+import { getApiKey } from "../api"
+import { CliAuthToken } from "../components/SignIn"
+
+import { FullScreenLoader } from "../components/Loader/FullScreenLoader"
+import { useUser } from "../contexts/UserContext"
+
+const CliAuthenticationPage: React.FC = () => {
+  const { me } = useUser(true)
+  const styles = useStyles()
+
+  const [apiKey, setApiKey] = useState<string | null>(null)
+
+  useEffect(() => {
+    if (me?.id) {
+      void getApiKey().then(({ key }) => {
+        setApiKey(key)
+      })
+    }
+  }, [me?.id])
+
+  if (!apiKey) {
+    return <FullScreenLoader />
+  }
+
+  return (
+    <div className={styles.root}>
+      <CliAuthToken sessionToken={apiKey} />
+    </div>
+  )
+}
+
+const useStyles = makeStyles(() => ({
+  root: {
+    width: "100vw",
+    height: "100vh",
+    display: "flex",
+    justifyContent: "center",
+    alignItems: "center",
+  },
+}))
+
+export default CliAuthenticationPage