diff --git a/src/libraries/System.Net.NameResolution/src/System/Net/Dns.cs b/src/libraries/System.Net.NameResolution/src/System/Net/Dns.cs
index 67c29760dea20b..fdac620bbf15df 100644
--- a/src/libraries/System.Net.NameResolution/src/System/Net/Dns.cs
+++ b/src/libraries/System.Net.NameResolution/src/System/Net/Dns.cs
@@ -419,6 +419,10 @@ private static bool ValidateAddressFamily(ref AddressFamily addressFamily, strin
         private const string Localhost = "localhost";
         private const string InvalidDomain = "invalid";
 
+        // Some systems (e.g. Android, some Linux distros) map ::1 to "ip6-localhost" instead of
+        // "localhost" in /etc/hosts, which causes getaddrinfo("localhost", AF_INET6) to fail with EAI_NONAME.
+        private const string IPv6Localhost = "ip6-localhost";
+
         /// <summary>
         /// Checks if the given host name matches a reserved name or is a subdomain of it.
         /// For example, IsReservedName("foo.localhost", "localhost") returns true.
@@ -550,7 +554,16 @@ private static object GetHostEntryOrAddressesCore(string hostName, bool justAddr
 
             if (fallbackToLocalhost)
             {
-                return GetHostEntryOrAddressesCore(Localhost, justAddresses, addressFamily);
+                try
+                {
+                    return GetHostEntryOrAddressesCore(Localhost, justAddresses, addressFamily);
+                }
+                catch (SocketException ex) when (addressFamily == AddressFamily.InterNetworkV6 && ex.SocketErrorCode == SocketError.HostNotFound)
+                {
+                    // Some systems map ::1 to "ip6-localhost" instead of "localhost" in /etc/hosts.
+                    if (NetEventSource.Log.IsEnabled()) NetEventSource.Info(Localhost, $"localhost IPv6 resolution failed, retrying with '{IPv6Localhost}'");
+                    return GetHostEntryOrAddressesCore(IPv6Localhost, justAddresses, addressFamily);
+                }
             }
 
             Debug.Assert(result is not null);
@@ -795,8 +808,7 @@ static async Task<T> CompleteAsync(Task task, string hostName, bool justAddresse
                         NameResolutionTelemetry.Log.AfterResolution(hostName, activity, answer: result, exception: null);
                         fallbackOccurred = true;
 
-                        // result is IPAddress[] so justAddresses is guaranteed true here.
-                        return await ((Task<T>)(Task)Dns.GetHostAddressesAsync(Localhost, addressFamily, cancellationToken)).ConfigureAwait(false);
+                        return await GetLocalhostAddressesAsync(addressFamily, cancellationToken).ConfigureAwait(false);
                     }
 
                     if (isLocalhostSubdomain && result is IPHostEntry entry && entry.AddressList.Length == 0)
@@ -805,8 +817,7 @@ static async Task<T> CompleteAsync(Task task, string hostName, bool justAddresse
                         NameResolutionTelemetry.Log.AfterResolution(hostName, activity, answer: result, exception: null);
                         fallbackOccurred = true;
 
-                        // result is IPHostEntry so justAddresses is guaranteed false here.
-                        return await ((Task<T>)(Task)Dns.GetHostEntryAsync(Localhost, addressFamily, cancellationToken)).ConfigureAwait(false);
+                        return await GetLocalhostEntryAsync(addressFamily, cancellationToken).ConfigureAwait(false);
                     }
 
                     return result;
@@ -818,9 +829,9 @@ static async Task<T> CompleteAsync(Task task, string hostName, bool justAddresse
                     NameResolutionTelemetry.Log.AfterResolution(hostName, activity, answer: null, exception: ex);
                     fallbackOccurred = true;
 
-                    return await ((Task<T>)(justAddresses
-                        ? (Task)Dns.GetHostAddressesAsync(Localhost, addressFamily, cancellationToken)
-                        : Dns.GetHostEntryAsync(Localhost, addressFamily, cancellationToken))).ConfigureAwait(false);
+                    return justAddresses
+                        ? await GetLocalhostAddressesAsync(addressFamily, cancellationToken).ConfigureAwait(false)
+                        : await GetLocalhostEntryAsync(addressFamily, cancellationToken).ConfigureAwait(false);
                 }
                 catch (Exception ex)
                 {
@@ -834,6 +845,35 @@ static async Task<T> CompleteAsync(Task task, string hostName, bool justAddresse
                         NameResolutionTelemetry.Log.AfterResolution(hostName, activity, answer: result, exception: exception);
                     }
                 }
+
+                // Resolves "localhost" with the given address family, returning addresses.
+                // If IPv6 resolution fails with HostNotFound, retries with "ip6-localhost"
+                // because some systems map ::1 to "ip6-localhost" instead of "localhost" in /etc/hosts.
+                static async Task<T> GetLocalhostAddressesAsync(AddressFamily family, CancellationToken cancellationToken)
+                {
+                    try
+                    {
+                        return await ((Task<T>)(Task)Dns.GetHostAddressesAsync(Localhost, family, cancellationToken)).ConfigureAwait(false);
+                    }
+                    catch (SocketException ex) when (family == AddressFamily.InterNetworkV6 && ex.SocketErrorCode == SocketError.HostNotFound)
+                    {
+                        if (NetEventSource.Log.IsEnabled()) NetEventSource.Info(Localhost, $"localhost IPv6 resolution failed, retrying with '{IPv6Localhost}'");
+                        return await ((Task<T>)(Task)Dns.GetHostAddressesAsync(IPv6Localhost, family, cancellationToken)).ConfigureAwait(false);
+                    }
+                }
+
+                static async Task<T> GetLocalhostEntryAsync(AddressFamily family, CancellationToken cancellationToken)
+                {
+                    try
+                    {
+                        return await ((Task<T>)(Task)Dns.GetHostEntryAsync(Localhost, family, cancellationToken)).ConfigureAwait(false);
+                    }
+                    catch (SocketException ex) when (family == AddressFamily.InterNetworkV6 && ex.SocketErrorCode == SocketError.HostNotFound)
+                    {
+                        if (NetEventSource.Log.IsEnabled()) NetEventSource.Info(Localhost, $"localhost IPv6 resolution failed, retrying with '{IPv6Localhost}'");
+                        return await ((Task<T>)(Task)Dns.GetHostEntryAsync(IPv6Localhost, family, cancellationToken)).ConfigureAwait(false);
+                    }
+                }
             }
         }
 
diff --git a/src/libraries/System.Net.NameResolution/tests/FunctionalTests/GetHostAddressesTest.cs b/src/libraries/System.Net.NameResolution/tests/FunctionalTests/GetHostAddressesTest.cs
index e98abe1ab53e2f..b91219cf6fed19 100644
--- a/src/libraries/System.Net.NameResolution/tests/FunctionalTests/GetHostAddressesTest.cs
+++ b/src/libraries/System.Net.NameResolution/tests/FunctionalTests/GetHostAddressesTest.cs
@@ -249,7 +249,6 @@ public async Task DnsGetHostAddresses_LocalhostSubdomain_ReturnsLoopback(string
         [Theory]
         [InlineData(AddressFamily.InterNetwork)]
         [InlineData(AddressFamily.InterNetworkV6)]
-        [ActiveIssue("https://github.com/dotnet/runtime/issues/124751", TestPlatforms.Android)]
         public async Task DnsGetHostAddresses_LocalhostSubdomain_RespectsAddressFamily(AddressFamily addressFamily)
         {
             // Skip IPv6 test if OS doesn't support it.
diff --git a/src/libraries/System.Net.NameResolution/tests/FunctionalTests/GetHostEntryTest.cs b/src/libraries/System.Net.NameResolution/tests/FunctionalTests/GetHostEntryTest.cs
index 58c8015a50bd70..e3cb7066eadc17 100644
--- a/src/libraries/System.Net.NameResolution/tests/FunctionalTests/GetHostEntryTest.cs
+++ b/src/libraries/System.Net.NameResolution/tests/FunctionalTests/GetHostEntryTest.cs
@@ -414,7 +414,6 @@ public async Task DnsGetHostEntry_LocalhostWithTrailingDot_ReturnsLoopback()
         [Theory]
         [InlineData(AddressFamily.InterNetwork)]
         [InlineData(AddressFamily.InterNetworkV6)]
-        [ActiveIssue("https://github.com/dotnet/runtime/issues/124751", TestPlatforms.Android)]
         public async Task DnsGetHostEntry_LocalhostSubdomain_RespectsAddressFamily(AddressFamily addressFamily)
         {
             // Skip IPv6 test if OS doesn't support it.