diff --git a/cli/gitssh.go b/cli/gitssh.go
index e36f5deadc3d2..b18b919f79515 100644
--- a/cli/gitssh.go
+++ b/cli/gitssh.go
@@ -1,9 +1,15 @@
 package cli
 
 import (
+	"bufio"
+	"bytes"
+	"context"
 	"fmt"
+	"io"
 	"os"
 	"os/exec"
+	"os/signal"
+	"path/filepath"
 	"strings"
 
 	"github.com/spf13/cobra"
@@ -13,16 +19,30 @@ import (
 )
 
 func gitssh() *cobra.Command {
-	return &cobra.Command{
+	cmd := &cobra.Command{
 		Use:    "gitssh",
 		Hidden: true,
 		Short:  `Wraps the "ssh" command and uses the coder gitssh key for authentication`,
 		RunE: func(cmd *cobra.Command, args []string) error {
+			ctx := cmd.Context()
+			env := os.Environ()
+
+			// Catch interrupt signals to ensure the temporary private
+			// key file is cleaned up on most cases.
+			ctx, stop := signal.NotifyContext(ctx, interruptSignals...)
+			defer stop()
+
+			// Early check so errors are reported immediately.
+			identityFiles, err := parseIdentityFilesForHost(ctx, args, env)
+			if err != nil {
+				return err
+			}
+
 			client, err := createAgentClient(cmd)
 			if err != nil {
 				return xerrors.Errorf("create agent client: %w", err)
 			}
-			key, err := client.AgentGitSSHKey(cmd.Context())
+			key, err := client.AgentGitSSHKey(ctx)
 			if err != nil {
 				return xerrors.Errorf("get agent git ssh token: %w", err)
 			}
@@ -44,8 +64,23 @@ func gitssh() *cobra.Command {
 				return xerrors.Errorf("close temp gitsshkey file: %w", err)
 			}
 
-			args = append([]string{"-i", privateKeyFile.Name()}, args...)
-			c := exec.CommandContext(cmd.Context(), "ssh", args...)
+			// Append our key, giving precedence to user keys. Note that
+			// OpenSSH server are typically configured with MaxAuthTries
+			// set to the default value of 6. This means that only the 6
+			// first keys can be tried. However, we will assume that if
+			// a user has configured 6+ keys for a host, they know what
+			// they're doing. This behavior is critical if a server has
+			// been configured with MaxAuthTries set to 1.
+			identityFiles = append(identityFiles, privateKeyFile.Name())
+
+			var identityArgs []string
+			for _, id := range identityFiles {
+				identityArgs = append(identityArgs, "-i", id)
+			}
+
+			args = append(identityArgs, args...)
+			c := exec.CommandContext(ctx, "ssh", args...)
+			c.Env = append(c.Env, env...)
 			c.Stderr = cmd.ErrOrStderr()
 			c.Stdout = cmd.OutOrStdout()
 			c.Stdin = cmd.InOrStdin()
@@ -69,4 +104,86 @@ func gitssh() *cobra.Command {
 			return nil
 		},
 	}
+
+	return cmd
+}
+
+// fallbackIdentityFiles is the list of identity files SSH tries when
+// none have been defined for a host.
+var fallbackIdentityFiles = strings.Join([]string{
+	"identityfile ~/.ssh/id_rsa",
+	"identityfile ~/.ssh/id_dsa",
+	"identityfile ~/.ssh/id_ecdsa",
+	"identityfile ~/.ssh/id_ecdsa_sk",
+	"identityfile ~/.ssh/id_ed25519",
+	"identityfile ~/.ssh/id_ed25519_sk",
+	"identityfile ~/.ssh/id_xmss",
+}, "\n")
+
+// parseIdentityFilesForHost uses ssh -G to discern what SSH keys have
+// been enabled for the host (via the users SSH config) and returns a
+// list of existing identity files.
+//
+// We do this because when no keys are defined for a host, SSH uses
+// fallback keys (see above). However, by passing `-i` to attach our
+// private key, we're effectively disabling the fallback keys.
+//
+// Example invocation:
+//
+//	ssh -G -o SendEnv=GIT_PROTOCOL git@github.com git-upload-pack 'coder/coder'
+//
+// The extra arguments work without issue and lets us run the command
+// as-is without stripping out the excess (git-upload-pack 'coder/coder').
+func parseIdentityFilesForHost(ctx context.Context, args, env []string) (identityFiles []string, error error) {
+	home, err := os.UserHomeDir()
+	if err != nil {
+		return nil, xerrors.Errorf("get user home dir failed: %w", err)
+	}
+
+	var outBuf bytes.Buffer
+	var r io.Reader = &outBuf
+
+	args = append([]string{"-G"}, args...)
+	cmd := exec.CommandContext(ctx, "ssh", args...)
+	cmd.Env = append(cmd.Env, env...)
+	cmd.Stdout = &outBuf
+	cmd.Stderr = io.Discard
+	err = cmd.Run()
+	if err != nil {
+		// If ssh -G failed, the SSH version is likely too old, fallback
+		// to using the default identity files.
+		r = strings.NewReader(fallbackIdentityFiles)
+	}
+
+	s := bufio.NewScanner(r)
+	for s.Scan() {
+		line := s.Text()
+		if strings.HasPrefix(line, "identityfile ") {
+			id := strings.TrimPrefix(line, "identityfile ")
+			if strings.HasPrefix(id, "~/") {
+				id = home + id[1:]
+			}
+			// OpenSSH on Windows is weird, it supports using (and does
+			// use) mixed \ and / in paths.
+			//
+			// Example: C:\Users\ZeroCool/.ssh/known_hosts
+			//
+			// To check the file existence in Go, though, we want to use
+			// proper Windows paths.
+			// OpenSSH is amazing, this will work on Windows too:
+			// C:\Users\ZeroCool/.ssh/id_rsa
+			id = filepath.FromSlash(id)
+
+			// Only include the identity file if it exists.
+			if _, err := os.Stat(id); err == nil {
+				identityFiles = append(identityFiles, id)
+			}
+		}
+	}
+	if err := s.Err(); err != nil {
+		// This should never happen, the check is for completeness.
+		return nil, xerrors.Errorf("scan ssh output: %w", err)
+	}
+
+	return identityFiles, nil
 }
diff --git a/cli/gitssh_test.go b/cli/gitssh_test.go
index cdbbe6bd1f4ff..a187566f61b11 100644
--- a/cli/gitssh_test.go
+++ b/cli/gitssh_test.go
@@ -2,8 +2,16 @@ package cli_test
 
 import (
 	"context"
+	"crypto/ecdsa"
+	"crypto/elliptic"
+	"crypto/rand"
+	"crypto/x509"
+	"encoding/pem"
 	"fmt"
 	"net"
+	"os"
+	"path/filepath"
+	"strings"
 	"sync/atomic"
 	"testing"
 
@@ -17,99 +25,245 @@ import (
 	"github.com/coder/coder/codersdk"
 	"github.com/coder/coder/provisioner/echo"
 	"github.com/coder/coder/provisionersdk/proto"
+	"github.com/coder/coder/pty/ptytest"
+	"github.com/coder/coder/testutil"
 )
 
+func prepareTestGitSSH(ctx context.Context, t *testing.T) (*codersdk.Client, string, gossh.PublicKey) {
+	t.Helper()
+
+	client := coderdtest.New(t, &coderdtest.Options{IncludeProvisionerDaemon: true})
+	user := coderdtest.CreateFirstUser(t, client)
+
+	ctx, cancel := context.WithCancel(ctx)
+	defer t.Cleanup(cancel) // Defer so that cancel is the first cleanup.
+
+	// get user public key
+	keypair, err := client.GitSSHKey(ctx, codersdk.Me)
+	require.NoError(t, err)
+	//nolint:dogsled
+	pubkey, _, _, _, err := gossh.ParseAuthorizedKey([]byte(keypair.PublicKey))
+	require.NoError(t, err)
+
+	// setup template
+	agentToken := uuid.NewString()
+	version := coderdtest.CreateTemplateVersion(t, client, user.OrganizationID, &echo.Responses{
+		Parse:           echo.ParseComplete,
+		ProvisionDryRun: echo.ProvisionComplete,
+		Provision: []*proto.Provision_Response{{
+			Type: &proto.Provision_Response_Complete{
+				Complete: &proto.Provision_Complete{
+					Resources: []*proto.Resource{{
+						Name: "somename",
+						Type: "someinstance",
+						Agents: []*proto.Agent{{
+							Auth: &proto.Agent_Token{
+								Token: agentToken,
+							},
+						}},
+					}},
+				},
+			},
+		}},
+	})
+	template := coderdtest.CreateTemplate(t, client, user.OrganizationID, version.ID)
+	coderdtest.AwaitTemplateVersionJob(t, client, version.ID)
+	workspace := coderdtest.CreateWorkspace(t, client, user.OrganizationID, template.ID)
+	coderdtest.AwaitWorkspaceBuildJob(t, client, workspace.LatestBuild.ID)
+
+	// start workspace agent
+	cmd, root := clitest.New(t, "agent", "--agent-token", agentToken, "--agent-url", client.URL.String(), "--wireguard=false")
+	agentClient := client
+	clitest.SetupConfig(t, agentClient, root)
+
+	errC := make(chan error, 1)
+	go func() {
+		errC <- cmd.ExecuteContext(ctx)
+	}()
+	t.Cleanup(func() { require.NoError(t, <-errC) })
+
+	coderdtest.AwaitWorkspaceAgents(t, client, workspace.LatestBuild.ID)
+	resources, err := client.WorkspaceResourcesByBuild(ctx, workspace.LatestBuild.ID)
+	require.NoError(t, err)
+	dialer, err := client.DialWorkspaceAgent(ctx, resources[0].Agents[0].ID, nil)
+	require.NoError(t, err)
+	defer dialer.Close()
+	_, err = dialer.Ping()
+	require.NoError(t, err)
+
+	return agentClient, agentToken, pubkey
+}
+
+func serveSSHForGitSSH(t *testing.T, handler func(ssh.Session), pubkeys ...gossh.PublicKey) *net.TCPAddr {
+	t.Helper()
+
+	// start ssh server
+	l, err := net.Listen("tcp", "localhost:0")
+	require.NoError(t, err)
+	t.Cleanup(func() { _ = l.Close() })
+
+	serveOpts := []ssh.Option{
+		ssh.PublicKeyAuth(func(ctx ssh.Context, key ssh.PublicKey) bool {
+			for _, pubkey := range pubkeys {
+				if ssh.KeysEqual(pubkey, key) {
+					return true
+				}
+			}
+			return false
+		}),
+	}
+	errC := make(chan error, 1)
+	go func() {
+		// as long as we get a successful session we don't care if the server errors
+		errC <- ssh.Serve(l, handler, serveOpts...)
+	}()
+	t.Cleanup(func() {
+		_ = l.Close() // Ensure server shutdown.
+		<-errC
+	})
+
+	// start ssh session
+	addr, ok := l.Addr().(*net.TCPAddr)
+	require.True(t, ok)
+
+	return addr
+}
+
+func writePrivateKeyToFile(t *testing.T, name string, key *ecdsa.PrivateKey) {
+	t.Helper()
+
+	b, err := x509.MarshalPKCS8PrivateKey(key)
+	require.NoError(t, err)
+	b = pem.EncodeToMemory(&pem.Block{
+		Type:  "PRIVATE KEY",
+		Bytes: b,
+	})
+
+	err = os.WriteFile(name, b, 0o600)
+	require.NoError(t, err)
+}
+
 func TestGitSSH(t *testing.T) {
 	t.Parallel()
 	t.Run("Dial", func(t *testing.T) {
 		t.Parallel()
-		client := coderdtest.New(t, &coderdtest.Options{IncludeProvisionerDaemon: true})
-		user := coderdtest.CreateFirstUser(t, client)
 
-		// get user public key
-		keypair, err := client.GitSSHKey(context.Background(), codersdk.Me)
-		require.NoError(t, err)
-		publicKey, _, _, _, err := gossh.ParseAuthorizedKey([]byte(keypair.PublicKey))
+		ctx, cancel := context.WithTimeout(context.Background(), testutil.WaitLong)
+		defer cancel()
+
+		client, token, pubkey := prepareTestGitSSH(ctx, t)
+		var inc int64
+		errC := make(chan error, 1)
+		addr := serveSSHForGitSSH(t, func(s ssh.Session) {
+			atomic.AddInt64(&inc, 1)
+			t.Log("got authenticated session")
+			select {
+			case errC <- s.Exit(0):
+			default:
+				t.Error("error channel is full")
+			}
+		}, pubkey)
+
+		// set to agent config dir
+		cmd, _ := clitest.New(t,
+			"gitssh",
+			"--agent-url", client.URL.String(),
+			"--agent-token", token,
+			"--",
+			fmt.Sprintf("-p%d", addr.Port),
+			"-o", "StrictHostKeyChecking=no",
+			"-o", "IdentitiesOnly=yes",
+			"127.0.0.1",
+		)
+		err := cmd.ExecuteContext(ctx)
 		require.NoError(t, err)
+		require.EqualValues(t, 1, inc)
 
-		// setup template
-		agentToken := uuid.NewString()
-		version := coderdtest.CreateTemplateVersion(t, client, user.OrganizationID, &echo.Responses{
-			Parse:           echo.ParseComplete,
-			ProvisionDryRun: echo.ProvisionComplete,
-			Provision: []*proto.Provision_Response{{
-				Type: &proto.Provision_Response_Complete{
-					Complete: &proto.Provision_Complete{
-						Resources: []*proto.Resource{{
-							Name: "somename",
-							Type: "someinstance",
-							Agents: []*proto.Agent{{
-								Auth: &proto.Agent_Token{
-									Token: agentToken,
-								},
-							}},
-						}},
-					},
-				},
-			}},
-		})
-		template := coderdtest.CreateTemplate(t, client, user.OrganizationID, version.ID)
-		coderdtest.AwaitTemplateVersionJob(t, client, version.ID)
-		workspace := coderdtest.CreateWorkspace(t, client, user.OrganizationID, template.ID)
-		coderdtest.AwaitWorkspaceBuildJob(t, client, workspace.LatestBuild.ID)
-
-		// start workspace agent
-		cmd, root := clitest.New(t, "agent", "--agent-token", agentToken, "--agent-url", client.URL.String(), "--wireguard=false")
-		agentClient := client
-		clitest.SetupConfig(t, agentClient, root)
-		ctx, cancelFunc := context.WithCancel(context.Background())
-		defer cancelFunc()
-		agentErrC := make(chan error)
-		go func() {
-			agentErrC <- cmd.ExecuteContext(ctx)
-		}()
-
-		coderdtest.AwaitWorkspaceAgents(t, client, workspace.LatestBuild.ID)
-		resources, err := client.WorkspaceResourcesByBuild(context.Background(), workspace.LatestBuild.ID)
+		err = <-errC
+		require.NoError(t, err, "error in agent execute")
+	})
+
+	t.Run("Local SSH Keys", func(t *testing.T) {
+		t.Parallel()
+
+		home := t.TempDir()
+		sshdir := filepath.Join(home, ".ssh")
+		err := os.MkdirAll(sshdir, 0o700)
 		require.NoError(t, err)
-		dialer, err := client.DialWorkspaceAgent(context.Background(), resources[0].Agents[0].ID, nil)
+
+		idFile := filepath.Join(sshdir, "id_ed25519")
+		privkey, err := ecdsa.GenerateKey(elliptic.P256(), rand.Reader)
 		require.NoError(t, err)
-		defer dialer.Close()
-		_, err = dialer.Ping()
+		localPubkey, err := gossh.NewPublicKey(&privkey.PublicKey)
 		require.NoError(t, err)
+		writePrivateKeyToFile(t, idFile, privkey)
+
+		ctx, cancel := context.WithTimeout(context.Background(), testutil.WaitLong)
+		defer cancel()
 
-		// start ssh server
-		l, err := net.Listen("tcp", "localhost:0")
+		client, token, coderPubkey := prepareTestGitSSH(ctx, t)
+
+		authkey := make(chan gossh.PublicKey, 1)
+		addr := serveSSHForGitSSH(t, func(s ssh.Session) {
+			t.Logf("authenticated with: %s", gossh.MarshalAuthorizedKey(s.PublicKey()))
+			select {
+			case authkey <- s.PublicKey():
+			default:
+				t.Error("authkey channel is full")
+			}
+		}, localPubkey, coderPubkey)
+
+		// Create a new config which sets an identity file.
+		config := filepath.Join(sshdir, "config")
+		knownHosts := filepath.Join(sshdir, "known_hosts")
+		err = os.WriteFile(config, []byte(strings.Join([]string{
+			"Host mytest",
+			"  HostName 127.0.0.1",
+			fmt.Sprintf("  Port %d", addr.Port),
+			"  StrictHostKeyChecking no",
+			"  UserKnownHostsFile=" + knownHosts,
+			"  IdentitiesOnly yes",
+			"  IdentityFile=" + idFile,
+		}, "\n")), 0o600)
 		require.NoError(t, err)
-		defer l.Close()
-		publicKeyOption := ssh.PublicKeyAuth(func(ctx ssh.Context, key ssh.PublicKey) bool {
-			return ssh.KeysEqual(publicKey, key)
-		})
-		var inc int64
-		sshErrC := make(chan error)
-		go func() {
-			// as long as we get a successful session we don't care if the server errors
-			_ = ssh.Serve(l, func(s ssh.Session) {
-				atomic.AddInt64(&inc, 1)
-				t.Log("got authenticated session")
-				sshErrC <- s.Exit(0)
-			}, publicKeyOption)
-		}()
-
-		// start ssh session
-		addr, ok := l.Addr().(*net.TCPAddr)
-		require.True(t, ok)
-		// set to agent config dir
-		gitsshCmd, _ := clitest.New(t, "gitssh", "--agent-url", agentClient.URL.String(), "--agent-token", agentToken, "--", fmt.Sprintf("-p%d", addr.Port), "-o", "StrictHostKeyChecking=no", "-o", "IdentitiesOnly=yes", "127.0.0.1")
-		err = gitsshCmd.ExecuteContext(context.Background())
+
+		pty := ptytest.New(t)
+		cmdArgs := []string{
+			"gitssh",
+			"--agent-url", client.URL.String(),
+			"--agent-token", token,
+			"--",
+			"-F", config,
+			"mytest",
+		}
+		// Test authentication via local private key.
+		cmd, _ := clitest.New(t, cmdArgs...)
+		cmd.SetOut(pty.Output())
+		cmd.SetErr(pty.Output())
+		err = cmd.ExecuteContext(ctx)
 		require.NoError(t, err)
-		require.EqualValues(t, 1, inc)
+		select {
+		case key := <-authkey:
+			require.Equal(t, localPubkey, key)
+		case <-ctx.Done():
+			t.Fatal("timeout waiting for auth")
+		}
 
-		err = <-sshErrC
-		require.NoError(t, err, "error in ssh session exit")
+		// Delete the local private key.
+		err = os.Remove(idFile)
+		require.NoError(t, err)
 
-		cancelFunc()
-		err = <-agentErrC
-		require.NoError(t, err, "error in agent execute")
+		// With the local file deleted, the coder key should be used.
+		cmd, _ = clitest.New(t, cmdArgs...)
+		cmd.SetOut(pty.Output())
+		cmd.SetErr(pty.Output())
+		err = cmd.ExecuteContext(ctx)
+		require.NoError(t, err)
+		select {
+		case key := <-authkey:
+			require.Equal(t, coderPubkey, key)
+		case <-ctx.Done():
+			t.Fatal("timeout waiting for auth")
+		}
 	})
 }