diff --git a/src/Servers/Kestrel/Core/src/Systemd/KestrelServerOptionsSystemdExtensions.cs b/src/Servers/Kestrel/Core/src/Systemd/KestrelServerOptionsSystemdExtensions.cs
index 6def39159de2..bf8f0fe69437 100644
--- a/src/Servers/Kestrel/Core/src/Systemd/KestrelServerOptionsSystemdExtensions.cs
+++ b/src/Servers/Kestrel/Core/src/Systemd/KestrelServerOptionsSystemdExtensions.cs
@@ -11,11 +11,12 @@ namespace Microsoft.AspNetCore.Hosting
     public static class KestrelServerOptionsSystemdExtensions
     {
         // SD_LISTEN_FDS_START https://www.freedesktop.org/software/systemd/man/sd_listen_fds.html
-        private const ulong SdListenFdsStart = 3;
+        private const int SdListenFdsStart = 3;
         private const string ListenPidEnvVar = "LISTEN_PID";
+        private const string ListenFdsEnvVar = "LISTEN_FDS";
 
         /// <summary>
-        /// Open file descriptor (SD_LISTEN_FDS_START) initialized by systemd socket-based activation logic if available.
+        /// Open file descriptors (starting from SD_LISTEN_FDS_START) initialized by systemd socket-based activation logic if available.
         /// </summary>
         /// <returns>
         /// The <see cref="KestrelServerOptions"/>.
@@ -26,7 +27,7 @@ public static KestrelServerOptions UseSystemd(this KestrelServerOptions options)
         }
 
         /// <summary>
-        /// Open file descriptor (SD_LISTEN_FDS_START) initialized by systemd socket-based activation logic if available.
+        /// Open file descriptors (starting from SD_LISTEN_FDS_START) initialized by systemd socket-based activation logic if available.
         /// Specify callback to configure endpoint-specific settings.
         /// </summary>
         /// <returns>
@@ -36,7 +37,16 @@ public static KestrelServerOptions UseSystemd(this KestrelServerOptions options,
         {
             if (string.Equals(Process.GetCurrentProcess().Id.ToString(CultureInfo.InvariantCulture), Environment.GetEnvironmentVariable(ListenPidEnvVar), StringComparison.Ordinal))
             {
-                options.ListenHandle(SdListenFdsStart, configure);
+                // This matches sd_listen_fds behavior that requires %LISTEN_FDS% to be present and in range [1;INT_MAX-SD_LISTEN_FDS_START]
+                if (int.TryParse(Environment.GetEnvironmentVariable(ListenFdsEnvVar), NumberStyles.None, NumberFormatInfo.InvariantInfo, out var listenFds)
+                    && listenFds > 0
+                    && listenFds <= int.MaxValue - SdListenFdsStart)
+                {
+                    for (var handle = SdListenFdsStart; handle < SdListenFdsStart + listenFds; ++handle)
+                    {
+                        options.ListenHandle((ulong)handle, configure);
+                    }
+                }
             }
 
             return options;