diff --git a/ee/tuf/library_lookup.go b/ee/tuf/library_lookup.go
index 19a0b22e4..240545dc8 100644
--- a/ee/tuf/library_lookup.go
+++ b/ee/tuf/library_lookup.go
@@ -13,6 +13,7 @@ import (
 	"github.com/kolide/launcher/pkg/launcher"
 	"github.com/kolide/launcher/pkg/traces"
 	"github.com/peterbourgon/ff/v3"
+	"github.com/spf13/pflag"
 )
 
 type BinaryUpdateInfo struct {
@@ -38,7 +39,7 @@ var channelsUsingNewAutoupdater = map[string]bool{
 // For now, it is only available when launcher is on the nightly update channel.
 func CheckOutLatestWithoutConfig(binary autoupdatableBinary, logger log.Logger) (*BinaryUpdateInfo, error) {
 	logger = log.With(logger, "component", "tuf_library_lookup")
-	cfg, err := getAutoupdateConfig()
+	cfg, err := getAutoupdateConfig(os.Args[1:])
 	if err != nil {
 		return nil, fmt.Errorf("could not get autoupdate config: %w", err)
 	}
@@ -52,7 +53,7 @@ func CheckOutLatestWithoutConfig(binary autoupdatableBinary, logger log.Logger)
 }
 
 func UsingNewAutoupdater() bool {
-	cfg, err := getAutoupdateConfig()
+	cfg, err := getAutoupdateConfig(os.Args[1:])
 	if err != nil {
 		return false
 	}
@@ -60,13 +61,53 @@ func UsingNewAutoupdater() bool {
 	return ChannelUsesNewAutoupdater(cfg.channel)
 }
 
-// getAutoupdateConfig reads launcher's config file to determine the configuration values
-// needed to work with the autoupdate library.
-func getAutoupdateConfig() (*autoupdateConfig, error) {
-	configFilePath := launcher.ConfigFilePath(os.Args[1:])
-	if configFilePath == "" {
-		return nil, errors.New("could not get config file path")
+// getAutoupdateConfig pulls the configuration values necessary to work with the autoupdate library
+// from either the given args or from the config file.
+func getAutoupdateConfig(args []string) (*autoupdateConfig, error) {
+	// Create a flagset with options that are relevant to autoupdate only.
+	// Ensure that we won't fail out when we see other command-line options.
+	pflagSet := pflag.NewFlagSet("autoupdate options", pflag.ContinueOnError)
+	pflagSet.ParseErrorsWhitelist = pflag.ParseErrorsWhitelist{UnknownFlags: true}
+
+	// Extract the config flag plus the autoupdate flags
+	var flConfigFilePath, flRootDirectory, flUpdateDirectory, flUpdateChannel, flLocalDevelopmentPath string
+	pflagSet.StringVar(&flConfigFilePath, "config", "", "")
+	pflagSet.StringVar(&flRootDirectory, "root_directory", "", "")
+	pflagSet.StringVar(&flUpdateDirectory, "update_directory", "", "")
+	pflagSet.StringVar(&flUpdateChannel, "update_channel", "", "")
+	pflagSet.StringVar(&flLocalDevelopmentPath, "localdev_path", "", "")
+
+	if err := pflagSet.Parse(args); err != nil {
+		return nil, fmt.Errorf("parsing command-line flags: %w", err)
+	}
+
+	// If the config file wasn't set AND the other critical flags weren't set, fall back
+	// to looking in the default config flag file location. (The update directory and local
+	// development path are both optional flags and not critical to library lookup
+	// functionality.) We expect all the flags to be set either via config flag (flConfigFilePath
+	// is set) or via command line (flRootDirectory and flUpdateChannel are set), but do not
+	// support a mix of both for this usage.
+	if flConfigFilePath == "" && flRootDirectory == "" && flUpdateChannel == "" {
+		return getAutoupdateConfigFromFile(launcher.ConfigFilePath(args))
+	}
+
+	if flConfigFilePath != "" {
+		return getAutoupdateConfigFromFile(flConfigFilePath)
 	}
+
+	cfg := &autoupdateConfig{
+		rootDirectory:        flRootDirectory,
+		updateDirectory:      flUpdateDirectory,
+		channel:              flUpdateChannel,
+		localDevelopmentPath: flLocalDevelopmentPath,
+	}
+
+	return cfg, nil
+}
+
+// getAutoupdateConfigFromFile reads launcher's config file to determine the configuration values
+// needed to work with the autoupdate library.
+func getAutoupdateConfigFromFile(configFilePath string) (*autoupdateConfig, error) {
 	if _, err := os.Stat(configFilePath); err != nil && os.IsNotExist(err) {
 		return nil, fmt.Errorf("could not read config file because it does not exist at %s: %w", configFilePath, err)
 	}
diff --git a/ee/tuf/library_lookup_test.go b/ee/tuf/library_lookup_test.go
index 55a09f73d..1fab2011d 100644
--- a/ee/tuf/library_lookup_test.go
+++ b/ee/tuf/library_lookup_test.go
@@ -214,3 +214,62 @@ func TestChannelUsesNewAutoupdater(t *testing.T) {
 		require.Equal(t, channel.usesNewAutoupdater, ChannelUsesNewAutoupdater(channel.channelName))
 	}
 }
+
+func Test_getAutoupdateConfig_ConfigFlagSet(t *testing.T) {
+	t.Parallel()
+
+	tempConfDir := t.TempDir()
+	configFilepath := filepath.Join(tempConfDir, "launcher.flags")
+
+	testRootDir := t.TempDir()
+	testChannel := "nightly"
+
+	fileContents := fmt.Sprintf(`
+with_initial_runner
+autoupdate
+hostname localhost
+root_directory %s
+update_channel %s
+transport jsonrpc
+`,
+		testRootDir,
+		testChannel,
+	)
+
+	require.NoError(t, os.WriteFile(configFilepath, []byte(fileContents), 0755), "expected to set up test config file")
+
+	cfg, err := getAutoupdateConfig([]string{"--config", configFilepath})
+	require.NoError(t, err, "expected no error getting autoupdate config")
+
+	require.NotNil(t, cfg, "expected valid autoupdate config")
+	require.Equal(t, testRootDir, cfg.rootDirectory, "root directory is incorrect")
+	require.Equal(t, "", cfg.updateDirectory, "update directory should not have been set")
+	require.Equal(t, testChannel, cfg.channel, "channel is incorrect")
+	require.Equal(t, "", cfg.localDevelopmentPath, "local development path should not have been set")
+}
+
+func Test_getAutoupdateConfig_ConfigFlagNotSet(t *testing.T) {
+	t.Parallel()
+
+	testRootDir := t.TempDir()
+	testUpdateDir := t.TempDir()
+	testChannel := "nightly"
+	testLocaldevPath := filepath.Join("some", "path", "to", "a", "local", "build")
+
+	cfg, err := getAutoupdateConfig([]string{
+		"--root_directory", testRootDir,
+		"--osquery_flag", "enable_watchdog_debug=true",
+		"--update_directory", testUpdateDir,
+		"--autoupdate",
+		"--update_channel", testChannel,
+		"--localdev_path", testLocaldevPath,
+		"--transport", "jsonrpc",
+	})
+	require.NoError(t, err, "expected no error getting autoupdate config")
+
+	require.NotNil(t, cfg, "expected valid autoupdate config")
+	require.Equal(t, testRootDir, cfg.rootDirectory, "root directory is incorrect")
+	require.Equal(t, testUpdateDir, cfg.updateDirectory, "update directory is incorrect")
+	require.Equal(t, testChannel, cfg.channel, "channel is incorrect")
+	require.Equal(t, testLocaldevPath, cfg.localDevelopmentPath, "local development path is incorrect")
+}
diff --git a/go.mod b/go.mod
index 3dbd290fd..6bd41b6c8 100644
--- a/go.mod
+++ b/go.mod
@@ -67,6 +67,7 @@ require (
 	github.com/felixge/httpsnoop v1.0.3 // indirect
 	github.com/grpc-ecosystem/grpc-gateway/v2 v2.18.0 // indirect
 	github.com/samber/lo v1.38.1 // indirect
+	github.com/spf13/pflag v1.0.5 // indirect
 	go.opentelemetry.io/proto/otlp v1.0.0 // indirect
 	golang.org/x/mod v0.14.0 // indirect
 	golang.org/x/tools v0.16.0 // indirect