diff --git a/docs/containers-auth.json.5.md b/docs/containers-auth.json.5.md
index 4030a06c05..5a15d310e4 100644
--- a/docs/containers-auth.json.5.md
+++ b/docs/containers-auth.json.5.md
@@ -6,15 +6,20 @@ containers-auth.json - syntax for the registry authentication file
 # DESCRIPTION
 
 A credentials file in JSON format used to authenticate against container image registries.
-The primary (read/write) file is stored at `${XDG_RUNTIME_DIR}/containers/auth.json` on Linux;
+The primary (read/write) per-user file is stored at `${XDG_RUNTIME_DIR}/containers/auth.json` on Linux;
 on Windows and macOS, at `$HOME/.config/containers/auth.json`.
 
-When searching for the credential for a registry, the following files will be read in sequence until the valid credential is found:
+There is also a system-global `/etc/containers/auth.json` path.  When the current process is executing inside systemd as root, this path will be preferred.
+
+When running as a user and searching for the credential for a registry, the following files will be read in sequence until the valid credential is found:
 first reading the primary (read/write) file, or the explicit override using an option of the calling application.
 If credentials are not present, search in `${XDG_CONFIG_HOME}/containers/auth.json` (usually `~/.config/containers/auth.json`), `$HOME/.docker/config.json`, `$HOME/.dockercfg`.
 
+If the current process is not running in systemd, but is running as root, the system global path will be read last.
+
 Except the primary (read/write) file, other files are read-only, unless the user use an option of the calling application explicitly points at it as an override.
 
+Note that the `/etc/containers/auth.json` file must not be readable by group or world (i.e. mode `044`), or a fatal error will occur.
 
 ## FORMAT
 
diff --git a/pkg/docker/config/config.go b/pkg/docker/config/config.go
index 6c9bca04eb..961ab8bd03 100644
--- a/pkg/docker/config/config.go
+++ b/pkg/docker/config/config.go
@@ -5,6 +5,7 @@ import (
 	"encoding/json"
 	"errors"
 	"fmt"
+	"io"
 	"os"
 	"os/exec"
 	"path/filepath"
@@ -32,6 +33,8 @@ type dockerConfigFile struct {
 	CredHelpers map[string]string           `json:"credHelpers,omitempty"`
 }
 
+// systemPath is the global auth path preferred for systemd services.
+var systemPath = authPath{path: filepath.FromSlash("/etc/containers/auth.json"), legacyFormat: false, requireUserOnly: true}
 var (
 	defaultPerUIDPathFormat = filepath.FromSlash("/run/containers/%d/auth.json")
 	xdgConfigHomePath       = filepath.FromSlash("containers/auth.json")
@@ -53,6 +56,8 @@ var (
 type authPath struct {
 	path         string
 	legacyFormat bool
+	// requireUserOnly will cause the file to be ignored if it is readable by group or other
+	requireUserOnly bool
 }
 
 // newAuthPathDefault constructs an authPath in non-legacy format.
@@ -215,7 +220,21 @@ func GetAllCredentials(sys *types.SystemContext) (map[string]types.DockerAuthCon
 // The homeDir parameter should always be homedir.Get(), and is only intended to be overridden
 // by tests.
 func getAuthFilePaths(sys *types.SystemContext, homeDir string) []authPath {
+	runningInSystemd := os.Getenv("INVOCATION_ID") != ""
+	runningAsRoot := os.Getuid() == 0
+	runningSystemdPrivileged := runningInSystemd && runningAsRoot
+
 	paths := []authPath{}
+
+	haveExplicitConfig := sys != nil && (sys.AuthFilePath != "" || sys.LegacyFormatAuthFilePath != "")
+
+	// If we're in systemd, prefer the global auth path first.
+	insertedGlobalPath := false
+	if !haveExplicitConfig && runningSystemdPrivileged {
+		paths = append(paths, systemPath)
+		insertedGlobalPath = true
+	}
+
 	pathToAuth, err := getPathToAuth(sys)
 	if err == nil {
 		paths = append(paths, pathToAuth)
@@ -225,7 +244,7 @@ func getAuthFilePaths(sys *types.SystemContext, homeDir string) []authPath {
 		// Logging the error as a warning instead and moving on to pulling the image
 		logrus.Warnf("%v: Trying to pull image in the event that it is a public image.", err)
 	}
-	if sys == nil || (sys.AuthFilePath == "" && sys.LegacyFormatAuthFilePath == "") {
+	if !haveExplicitConfig {
 		xdgCfgHome := os.Getenv("XDG_CONFIG_HOME")
 		if xdgCfgHome == "" {
 			xdgCfgHome = filepath.Join(homeDir, ".config")
@@ -241,6 +260,12 @@ func getAuthFilePaths(sys *types.SystemContext, homeDir string) []authPath {
 		paths = append(paths,
 			authPath{path: filepath.Join(homeDir, dockerLegacyHomePath), legacyFormat: true},
 		)
+		// If we didn't already insert the global path, do it at the end if we're running as root.
+		// This will ensure the same semantics for code executed as systemd units and run
+		// from an interactive shell (as root) as long as there's no user-root owned configs.
+		if !insertedGlobalPath && runningAsRoot {
+			paths = append(paths, systemPath)
+		}
 	}
 	return paths
 }
@@ -552,7 +577,7 @@ func getPathToAuthWithOS(sys *types.SystemContext, goOS string) (authPath, error
 func (path authPath) parse() (dockerConfigFile, error) {
 	var auths dockerConfigFile
 
-	raw, err := os.ReadFile(path.path)
+	f, err := os.Open(path.path)
 	if err != nil {
 		if os.IsNotExist(err) {
 			auths.AuthConfigs = map[string]dockerAuthConfig{}
@@ -560,6 +585,21 @@ func (path authPath) parse() (dockerConfigFile, error) {
 		}
 		return dockerConfigFile{}, err
 	}
+	defer f.Close()
+	if path.requireUserOnly {
+		st, err := f.Stat()
+		if err != nil {
+			return dockerConfigFile{}, fmt.Errorf("stat %s: %w", path.path, err)
+		}
+		perms := st.Mode().Perm()
+		if (perms & 044) > 0 {
+			return dockerConfigFile{}, fmt.Errorf("refusing to process %s with group or world read permissions", path.path)
+		}
+	}
+	raw, err := io.ReadAll(f)
+	if err != nil {
+		return dockerConfigFile{}, fmt.Errorf("reading %s: %w", path.path, err)
+	}
 
 	if path.legacyFormat {
 		if err = json.Unmarshal(raw, &auths.AuthConfigs); err != nil {