diff --git a/injectproxy/routes.go b/injectproxy/routes.go
index 4f93f977..30e18a60 100644
--- a/injectproxy/routes.go
+++ b/injectproxy/routes.go
@@ -234,7 +234,8 @@ func (hff HTTPFormEnforcer) getLabelValues(r *http.Request) ([]string, error) {
 
 // HTTPHeaderEnforcer enforces a label value extracted from the HTTP headers.
 type HTTPHeaderEnforcer struct {
-	Name string
+	Name            string
+	ParseListSyntax bool
 }
 
 // ExtractLabel implements the ExtractLabeler interface.
@@ -251,7 +252,13 @@ func (hhe HTTPHeaderEnforcer) ExtractLabel(next http.HandlerFunc) http.Handler {
 }
 
 func (hhe HTTPHeaderEnforcer) getLabelValues(r *http.Request) ([]string, error) {
-	headerValues := removeEmptyValues(r.Header[hhe.Name])
+	headerValues := r.Header[hhe.Name]
+
+	if hhe.ParseListSyntax {
+		headerValues = trimValues(splitValues(headerValues, ","))
+	}
+
+	headerValues = removeEmptyValues(headerValues)
 
 	if len(headerValues) == 0 {
 		return nil, fmt.Errorf("missing HTTP header %q", hhe.Name)
@@ -670,6 +677,18 @@ func humanFriendlyErrorMessage(err error) string {
 	return fmt.Sprintf("%s%s.", strings.ToUpper(errMsg[:1]), errMsg[1:])
 }
 
+func splitValues(slice []string, sep string) []string {
+	for i := 0; i < len(slice); {
+		splitResult := strings.Split(slice[i], sep)
+
+		slice = append(slice[:i], append(splitResult, slice[i+1:]...)...)
+
+		i += len(splitResult)
+	}
+
+	return slice
+}
+
 func removeEmptyValues(slice []string) []string {
 	for i := 0; i < len(slice); i++ {
 		if slice[i] == "" {
@@ -680,3 +699,11 @@ func removeEmptyValues(slice []string) []string {
 
 	return slice
 }
+
+func trimValues(slice []string) []string {
+	for i := 0; i < len(slice); i++ {
+		slice[i] = strings.TrimSpace(slice[i])
+	}
+
+	return slice
+}
diff --git a/injectproxy/routes_test.go b/injectproxy/routes_test.go
index 84836eb0..ead8e241 100644
--- a/injectproxy/routes_test.go
+++ b/injectproxy/routes_test.go
@@ -808,12 +808,13 @@ func TestQuery(t *testing.T) {
 		promQueryBody  string
 		method         string
 
-		expCode          int
-		expPromQuery     string
-		expPromQueryBody string
-		expResponse      []byte
-		errorOnReplace   bool
-		regexMatch       bool
+		expCode              int
+		expPromQuery         string
+		expPromQueryBody     string
+		expResponse          []byte
+		errorOnReplace       bool
+		regexMatch           bool
+		headerUsesListSyntax bool
 	}{
 		{
 			name:    `No "namespace" parameter returns an error`,
@@ -1104,6 +1105,28 @@ func TestQuery(t *testing.T) {
 			expPromQuery: `up{instance="localhost:9090",namespace=~"default|second"} + foo{namespace="second",namespace=~"default|second"}`,
 			expResponse:  okResponse,
 		},
+		{
+			name:         `HTTP header label with comma-separated values and list parsing disabled`,
+			headers:      http.Header{"namespace": []string{"default, second", "third"}},
+			headerName:   "namespace",
+			promQuery:    `up{instance="localhost:9090"} + foo{namespace="second"}`,
+			expCode:      http.StatusOK,
+			expPromQuery: `up{instance="localhost:9090",namespace=~"default, second|third"} + foo{namespace="second",namespace=~"default, second|third"}`,
+			expResponse:  okResponse,
+
+			headerUsesListSyntax: false,
+		},
+		{
+			name:         `HTTP header label with comma-separated values and list parsing enabled`,
+			headers:      http.Header{"namespace": []string{"default, second", "third"}},
+			headerName:   "namespace",
+			promQuery:    `up{instance="localhost:9090"} + foo{namespace="second"}`,
+			expCode:      http.StatusOK,
+			expPromQuery: `up{instance="localhost:9090",namespace=~"default|second|third"} + foo{namespace="second",namespace=~"default|second|third"}`,
+			expResponse:  okResponse,
+
+			headerUsesListSyntax: true,
+		},
 		{
 			name:         `multiple HTTP header with empty label value`,
 			headers:      http.Header{"namespace": []string{"default", ""}},
@@ -1203,7 +1226,7 @@ func TestQuery(t *testing.T) {
 				if len(tc.staticLabelVal) > 0 {
 					labelEnforcer = StaticLabelEnforcer(tc.staticLabelVal)
 				} else if tc.headerName != "" {
-					labelEnforcer = HTTPHeaderEnforcer{Name: tc.headerName}
+					labelEnforcer = HTTPHeaderEnforcer{Name: tc.headerName, ParseListSyntax: tc.headerUsesListSyntax}
 				} else if tc.queryParam != "" {
 					labelEnforcer = HTTPFormEnforcer{ParameterName: tc.queryParam}
 				} else {
diff --git a/main.go b/main.go
index 0f6b19cd..4d3b05eb 100644
--- a/main.go
+++ b/main.go
@@ -66,6 +66,7 @@ func main() {
 		unsafePassthroughPaths string // Comma-delimited string.
 		errorOnReplace         bool
 		regexMatch             bool
+		headerUsesListSyntax   bool
 	)
 
 	flagset := flag.NewFlagSet(os.Args[0], flag.ExitOnError)
@@ -84,6 +85,7 @@ func main() {
 		"API (like /api/v1/configuration) which isn't enforced by prom-label-proxy. NOTE: \"all\" matching paths like \"/\" or \"\" and regex are not allowed.")
 	flagset.BoolVar(&errorOnReplace, "error-on-replace", false, "When specified, the proxy will return HTTP status code 400 if the query already contains a label matcher that differs from the one the proxy would inject.")
 	flagset.BoolVar(&regexMatch, "regex-match", false, "When specified, the tenant name is treated as a regular expression. In this case, only one tenant name should be provided.")
+	flagset.BoolVar(&headerUsesListSyntax, "header-uses-list-syntax", false, "When specified, the header line value will be parsed as a comma-separated list. This allows a single tenant header line to specify multiple tenant names.")
 
 	//nolint: errcheck // Parse() will exit on error.
 	flagset.Parse(os.Args[1:])
@@ -154,7 +156,7 @@ func main() {
 	case queryParam != "":
 		extractLabeler = injectproxy.HTTPFormEnforcer{ParameterName: queryParam}
 	case headerName != "":
-		extractLabeler = injectproxy.HTTPHeaderEnforcer{Name: http.CanonicalHeaderKey(headerName)}
+		extractLabeler = injectproxy.HTTPHeaderEnforcer{Name: http.CanonicalHeaderKey(headerName), ParseListSyntax: headerUsesListSyntax}
 	}
 
 	var g run.Group