diff --git a/cli-plugins/examples/helloworld/main.go b/cli-plugins/examples/helloworld/main.go
index a319ee623f6c..e79e32ce5436 100644
--- a/cli-plugins/examples/helloworld/main.go
+++ b/cli-plugins/examples/helloworld/main.go
@@ -33,6 +33,6 @@ func main() {
 		manager.Metadata{
 			SchemaVersion: "0.1.0",
 			Vendor:        "Docker Inc.",
-			Version:       "0.1.0",
+			Version:       "testing",
 		})
 }
diff --git a/cli-plugins/manager/candidate.go b/cli-plugins/manager/candidate.go
new file mode 100644
index 000000000000..2000e5b142f6
--- /dev/null
+++ b/cli-plugins/manager/candidate.go
@@ -0,0 +1,23 @@
+package manager
+
+import (
+	"os/exec"
+)
+
+// Candidate represents a possible plugin candidate, for mocking purposes
+type Candidate interface {
+	Path() string
+	Metadata() ([]byte, error)
+}
+
+type candidate struct {
+	path string
+}
+
+func (c *candidate) Path() string {
+	return c.path
+}
+
+func (c *candidate) Metadata() ([]byte, error) {
+	return exec.Command(c.path, MetadataSubcommandName).Output()
+}
diff --git a/cli-plugins/manager/candidate_test.go b/cli-plugins/manager/candidate_test.go
new file mode 100644
index 000000000000..11384226a5d4
--- /dev/null
+++ b/cli-plugins/manager/candidate_test.go
@@ -0,0 +1,90 @@
+package manager
+
+import (
+	"fmt"
+	"strings"
+	"testing"
+
+	"github.com/spf13/cobra"
+	"gotest.tools/assert"
+)
+
+type fakeCandidate struct {
+	path string
+	exec bool
+	meta string
+}
+
+func (c *fakeCandidate) Path() string {
+	return c.path
+}
+
+func (c *fakeCandidate) Metadata() ([]byte, error) {
+	if !c.exec {
+		return nil, fmt.Errorf("faked a failure to exec %q", c.path)
+	}
+	return []byte(c.meta), nil
+}
+
+func TestValidateCandidate(t *testing.T) {
+	var (
+		goodPluginName = NamePrefix + "goodplugin"
+
+		builtinName  = NamePrefix + "builtin"
+		builtinAlias = NamePrefix + "alias"
+
+		badPrefixPath  = "/usr/local/libexec/cli-plugins/wobble"
+		badNamePath    = "/usr/local/libexec/cli-plugins/docker-123456"
+		goodPluginPath = "/usr/local/libexec/cli-plugins/" + goodPluginName
+	)
+
+	fakeroot := &cobra.Command{Use: "docker"}
+	fakeroot.AddCommand(&cobra.Command{
+		Use: strings.TrimPrefix(builtinName, NamePrefix),
+		Aliases: []string{
+			strings.TrimPrefix(builtinAlias, NamePrefix),
+		},
+	})
+
+	for _, tc := range []struct {
+		c *fakeCandidate
+
+		// Either err or invalid may be non-empty, but not both (both can be empty for a good plugin).
+		err     string
+		invalid string
+	}{
+		/* Each failing one of the tests */
+		{c: &fakeCandidate{path: ""}, err: "plugin candidate path cannot be empty"},
+		{c: &fakeCandidate{path: badPrefixPath}, err: fmt.Sprintf("does not have %q prefix", NamePrefix)},
+		{c: &fakeCandidate{path: badNamePath}, invalid: "did not match"},
+		{c: &fakeCandidate{path: builtinName}, invalid: `plugin "builtin" duplicates builtin command`},
+		{c: &fakeCandidate{path: builtinAlias}, invalid: `plugin "alias" duplicates an alias of builtin command "builtin"`},
+		{c: &fakeCandidate{path: goodPluginPath, exec: false}, invalid: fmt.Sprintf("failed to fetch metadata: faked a failure to exec %q", goodPluginPath)},
+		{c: &fakeCandidate{path: goodPluginPath, exec: true, meta: `xyzzy`}, invalid: "invalid character"},
+		{c: &fakeCandidate{path: goodPluginPath, exec: true, meta: `{}`}, invalid: `plugin SchemaVersion "" is not valid`},
+		{c: &fakeCandidate{path: goodPluginPath, exec: true, meta: `{"SchemaVersion": "xyzzy"}`}, invalid: `plugin SchemaVersion "xyzzy" is not valid`},
+		{c: &fakeCandidate{path: goodPluginPath, exec: true, meta: `{"SchemaVersion": "0.1.0"}`}, invalid: "plugin metadata does not define a vendor"},
+		{c: &fakeCandidate{path: goodPluginPath, exec: true, meta: `{"SchemaVersion": "0.1.0", "Vendor": ""}`}, invalid: "plugin metadata does not define a vendor"},
+		// This one should work
+		{c: &fakeCandidate{path: goodPluginPath, exec: true, meta: `{"SchemaVersion": "0.1.0", "Vendor": "e2e-testing"}`}},
+	} {
+		p, err := newPlugin(tc.c, fakeroot)
+		if tc.err != "" {
+			assert.ErrorContains(t, err, tc.err)
+		} else if tc.invalid != "" {
+			assert.NilError(t, err)
+			assert.ErrorContains(t, p.Err, tc.invalid)
+		} else {
+			assert.NilError(t, err)
+			assert.Equal(t, NamePrefix+p.Name, goodPluginName)
+			assert.Equal(t, p.SchemaVersion, "0.1.0")
+			assert.Equal(t, p.Vendor, "e2e-testing")
+		}
+	}
+}
+
+func TestCandidatePath(t *testing.T) {
+	exp := "/some/path"
+	cand := &candidate{path: exp}
+	assert.Equal(t, exp, cand.Path())
+}
diff --git a/cli-plugins/manager/manager.go b/cli-plugins/manager/manager.go
new file mode 100644
index 000000000000..882d2ee2ea98
--- /dev/null
+++ b/cli-plugins/manager/manager.go
@@ -0,0 +1,93 @@
+package manager
+
+import (
+	"os"
+	"os/exec"
+	"path/filepath"
+	"runtime"
+
+	"github.com/docker/cli/cli/command"
+	"github.com/docker/cli/cli/config"
+	"github.com/spf13/cobra"
+)
+
+// errPluginNotFound is the error returned when a plugin could not be found.
+type errPluginNotFound string
+
+func (e errPluginNotFound) NotFound() {}
+
+func (e errPluginNotFound) Error() string {
+	return "Error: No such CLI plugin: " + string(e)
+}
+
+type notFound interface{ NotFound() }
+
+// IsNotFound is true if the given error is due to a plugin not being found.
+func IsNotFound(err error) bool {
+	_, ok := err.(notFound)
+	return ok
+}
+
+var defaultUserPluginDir = config.Path("cli-plugins")
+
+func getPluginDirs(dockerCli command.Cli) []string {
+	var pluginDirs []string
+
+	if cfg := dockerCli.ConfigFile(); cfg != nil {
+		pluginDirs = append(pluginDirs, cfg.CLIPluginsExtraDirs...)
+	}
+	pluginDirs = append(pluginDirs, defaultUserPluginDir)
+	pluginDirs = append(pluginDirs, defaultSystemPluginDirs...)
+	return pluginDirs
+}
+
+// PluginRunCommand returns an "os/exec".Cmd which when .Run() will execute the named plugin.
+// The rootcmd argument is referenced to determine the set of builtin commands in order to detect conficts.
+// The error returned satisfies the IsNotFound() predicate if no plugin was found or if the first candidate plugin was invalid somehow.
+func PluginRunCommand(dockerCli command.Cli, name string, rootcmd *cobra.Command) (*exec.Cmd, error) {
+	// This uses the full original args, not the args which may
+	// have been provided by cobra to our caller. This is because
+	// they lack e.g. global options which we must propagate here.
+	args := os.Args[1:]
+	if !pluginNameRe.MatchString(name) {
+		// We treat this as "not found" so that callers will
+		// fallback to their "invalid" command path.
+		return nil, errPluginNotFound(name)
+	}
+	exename := NamePrefix + name
+	if runtime.GOOS == "windows" {
+		exename = exename + ".exe"
+	}
+	for _, d := range getPluginDirs(dockerCli) {
+		path := filepath.Join(d, exename)
+
+		// We stat here rather than letting the exec tell us
+		// ENOENT because the latter does not distinguish a
+		// file not existing from its dynamic loader or one of
+		// its libraries not existing.
+		if _, err := os.Stat(path); os.IsNotExist(err) {
+			continue
+		}
+
+		c := &candidate{path: path}
+		plugin, err := newPlugin(c, rootcmd)
+		if err != nil {
+			return nil, err
+		}
+		if plugin.Err != nil {
+			return nil, errPluginNotFound(name)
+		}
+		cmd := exec.Command(plugin.Path, args...)
+		// Using dockerCli.{In,Out,Err}() here results in a hang until something is input.
+		// See: - https://github.com/golang/go/issues/10338
+		//      - https://github.com/golang/go/commit/d000e8742a173aa0659584aa01b7ba2834ba28ab
+		// os.Stdin is a *os.File which avoids this behaviour. We don't need the functionality
+		// of the wrappers here anyway.
+		cmd.Stdin = os.Stdin
+		cmd.Stdout = os.Stdout
+		cmd.Stderr = os.Stderr
+
+		return cmd, nil
+	}
+	return nil, errPluginNotFound(name)
+}
diff --git a/cli-plugins/manager/manager_test.go b/cli-plugins/manager/manager_test.go
new file mode 100644
index 000000000000..3a62b911fab1
--- /dev/null
+++ b/cli-plugins/manager/manager_test.go
@@ -0,0 +1,36 @@
+package manager
+
+import (
+	"strings"
+	"testing"
+
+	"github.com/docker/cli/cli/config/configfile"
+	"github.com/docker/cli/internal/test"
+	"gotest.tools/assert"
+)
+
+func TestErrPluginNotFound(t *testing.T) {
+	var err error = errPluginNotFound("test")
+	err.(errPluginNotFound).NotFound()
+	assert.Error(t, err, "Error: No such CLI plugin: test")
+	assert.Assert(t, IsNotFound(err))
+	assert.Assert(t, !IsNotFound(nil))
+}
+
+func TestGetPluginDirs(t *testing.T) {
+	cli := test.NewFakeCli(nil)
+
+	expected := []string{defaultUserPluginDir}
+	expected = append(expected, defaultSystemPluginDirs...)
+
+	assert.Equal(t, strings.Join(expected, ":"), strings.Join(getPluginDirs(cli), ":"))
+
+	extras := []string{
+		"foo", "bar", "baz",
+	}
+	expected = append(extras, expected...)
+	cli.SetConfigFile(&configfile.ConfigFile{
+		CLIPluginsExtraDirs: extras,
+	})
+	assert.DeepEqual(t, expected, getPluginDirs(cli))
+}
diff --git a/cli-plugins/manager/manager_unix.go b/cli-plugins/manager/manager_unix.go
new file mode 100644
index 000000000000..f586acbd8da2
--- /dev/null
+++ b/cli-plugins/manager/manager_unix.go
@@ -0,0 +1,8 @@
+// +build !windows
+
+package manager
+
+var defaultSystemPluginDirs = []string{
+	"/usr/local/lib/docker/cli-plugins", "/usr/local/libexec/docker/cli-plugins",
+	"/usr/lib/docker/cli-plugins", "/usr/libexec/docker/cli-plugins",
+}
diff --git a/cli-plugins/manager/manager_windows.go b/cli-plugins/manager/manager_windows.go
new file mode 100644
index 000000000000..b62868580360
--- /dev/null
+++ b/cli-plugins/manager/manager_windows.go
@@ -0,0 +1,10 @@
+package manager
+
+import (
+	"os"
+	"path/filepath"
+)
+
+var defaultSystemPluginDirs = []string{
+	filepath.Join(os.Getenv("ProgramData"), "Docker", "cli-plugins"),
+}
diff --git a/cli-plugins/manager/plugin.go b/cli-plugins/manager/plugin.go
new file mode 100644
index 000000000000..8a07c5853726
--- /dev/null
+++ b/cli-plugins/manager/plugin.go
@@ -0,0 +1,104 @@
+package manager
+
+import (
+	"encoding/json"
+	"path/filepath"
+	"regexp"
+	"runtime"
+	"strings"
+
+	"github.com/pkg/errors"
+	"github.com/spf13/cobra"
+)
+
+var (
+	pluginNameRe = regexp.MustCompile("^[a-z][a-z0-9]*$")
+)
+
+// Plugin represents a potential plugin with all it's metadata.
+type Plugin struct {
+	Metadata
+
+	Name string
+	Path string
+
+	// Err is non-nil if the plugin failed one of the candidate tests.
+	Err error `json:",omitempty"`
+
+	// ShadowedPaths contains the paths of any other plugins which this plugin takes precedence over.
+	ShadowedPaths []string `json:",omitempty"`
+}
+
+// newPlugin determines if the given candidate is valid and returns a
+// Plugin.  If the candidate fails one of the tests then `Plugin.Err`
+// is set, but the `Plugin` is still returned with no error. An error
+// is only returned due to a non-recoverable error.
+func newPlugin(c Candidate, rootcmd *cobra.Command) (Plugin, error) {
+	path := c.Path()
+	if path == "" {
+		return Plugin{}, errors.New("plugin candidate path cannot be empty")
+	}
+
+	// The candidate listing process should have skipped anything
+	// which would fail here, so there are all real errors.
+	fullname := filepath.Base(path)
+	if fullname == "." {
+		return Plugin{}, errors.Errorf("unable to determine basename of plugin candidate %q", path)
+	}
+	if runtime.GOOS == "windows" {
+		exe := ".exe"
+		if !strings.HasSuffix(fullname, exe) {
+			return Plugin{}, errors.Errorf("plugin candidate %q lacks required %q suffix", path, exe)
+		}
+		fullname = strings.TrimSuffix(fullname, exe)
+	}
+	if !strings.HasPrefix(fullname, NamePrefix) {
+		return Plugin{}, errors.Errorf("plugin candidate %q does not have %q prefix", path, NamePrefix)
+	}
+
+	p := Plugin{
+		Name: strings.TrimPrefix(fullname, NamePrefix),
+		Path: path,
+	}
+
+	// Now apply the candidate tests, so these update p.Err.
+	if !pluginNameRe.MatchString(p.Name) {
+		p.Err = errors.Errorf("plugin candidate %q did not match %q", p.Name, pluginNameRe.String())
+		return p, nil
+	}
+
+	if rootcmd != nil {
+		for _, cmd := range rootcmd.Commands() {
+			if cmd.Name() == p.Name {
+				p.Err = errors.Errorf("plugin %q duplicates builtin command", p.Name)
+				return p, nil
+			}
+			if cmd.HasAlias(p.Name) {
+				p.Err = errors.Errorf("plugin %q duplicates an alias of builtin command %q", p.Name, cmd.Name())
+				return p, nil
+			}
+		}
+	}
+
+	// We are supposed to check for relevant execute permissions here. Instead we rely on an attempt to execute.
+	meta, err := c.Metadata()
+	if err != nil {
+		p.Err = errors.Wrap(err, "failed to fetch metadata")
+		return p, nil
+	}
+
+	if err := json.Unmarshal(meta, &p.Metadata); err != nil {
+		p.Err = errors.Wrap(err, "invalid metadata")
+		return p, nil
+	}
+
+	if p.Metadata.SchemaVersion != "0.1.0" {
+		p.Err = errors.Errorf("plugin SchemaVersion %q is not valid, must be 0.1.0", p.Metadata.SchemaVersion)
+		return p, nil
+	}
+	if p.Metadata.Vendor == "" {
+		p.Err = errors.Errorf("plugin metadata does not define a vendor")
+		return p, nil
+	}
+	return p, nil
+}
diff --git a/cli/config/configfile/file.go b/cli/config/configfile/file.go
index d815570362a8..99ffd47a5fcb 100644
--- a/cli/config/configfile/file.go
+++ b/cli/config/configfile/file.go
@@ -49,6 +49,7 @@ type ConfigFile struct {
 	StackOrchestrator    string                      `json:"stackOrchestrator,omitempty"`
 	Kubernetes           *KubernetesConfig           `json:"kubernetes,omitempty"`
 	CurrentContext       string                      `json:"currentContext,omitempty"`
+	CLIPluginsExtraDirs  []string                    `json:"cliPluginsExtraDirs,omitempty"`
 }
 
 // ProxyConfig contains proxy configuration settings
diff --git a/cmd/docker/docker.go b/cmd/docker/docker.go
index f8890304ecfb..062cbfdc9b73 100644
--- a/cmd/docker/docker.go
+++ b/cmd/docker/docker.go
@@ -7,6 +7,7 @@ import (
 	"strings"
 
 	"github.com/docker/cli/cli"
+	pluginmanager "github.com/docker/cli/cli-plugins/manager"
 	"github.com/docker/cli/cli/command"
 	"github.com/docker/cli/cli/command/commands"
 	cliflags "github.com/docker/cli/cli/flags"
@@ -30,9 +31,20 @@ func newDockerCommand(dockerCli *command.DockerCli) *cobra.Command {
 		SilenceUsage:     true,
 		SilenceErrors:    true,
 		TraverseChildren: true,
-		Args:             noArgs,
 		RunE: func(cmd *cobra.Command, args []string) error {
-			return command.ShowHelp(dockerCli.Err())(cmd, args)
+			if len(args) == 0 {
+				return command.ShowHelp(dockerCli.Err())(cmd, args)
+			}
+			plugincmd, err := pluginmanager.PluginRunCommand(dockerCli, args[0], cmd)
+			if pluginmanager.IsNotFound(err) {
+				return fmt.Errorf(
+					"docker: '%s' is not a docker command.\nSee 'docker --help'", args[0])
+			}
+			if err != nil {
+				return err
+			}
+
+			return plugincmd.Run()
 		},
 		PersistentPreRunE: func(cmd *cobra.Command, args []string) error {
 			// flags must be the top-level command flags, not cmd.Flags()
@@ -136,14 +148,6 @@ func initializeDockerCli(dockerCli *command.DockerCli, flags *pflag.FlagSet, opt
 	return dockerCli.Initialize(opts)
 }
 
-func noArgs(cmd *cobra.Command, args []string) error {
-	if len(args) == 0 {
-		return nil
-	}
-	return fmt.Errorf(
-		"docker: '%s' is not a docker command.\nSee 'docker --help'", args[0])
-}
-
 func main() {
 	dockerCli, err := command.NewDockerCli()
 	if err != nil {