diff --git a/daemon/libnetwork/internal/resolvconf/resolvconf.go b/daemon/libnetwork/internal/resolvconf/resolvconf.go
index 1df28ae0f2..6c8b2523c4 100644
--- a/daemon/libnetwork/internal/resolvconf/resolvconf.go
+++ b/daemon/libnetwork/internal/resolvconf/resolvconf.go
@@ -18,6 +18,7 @@ import (
 	"bufio"
 	"bytes"
 	"context"
+	"fmt"
 	"io"
 	"io/fs"
 	"net/netip"
@@ -115,7 +116,15 @@ func Parse(reader io.Reader, path string) (ResolvConf, error) {
 		rc.processLine(scanner.Text())
 	}
 	if err := scanner.Err(); err != nil {
-		return ResolvConf{}, systemError{err}
+		src := rc.md.SourcePath
+		if errors.Is(err, bufio.ErrTooLong) {
+			return ResolvConf{}, systemError{
+				fmt.Errorf("failed to parse resolv.conf from %s: line too long (exceeds %d)", src, bufio.MaxScanTokenSize),
+			}
+		}
+		return ResolvConf{}, systemError{
+			fmt.Errorf("failed to parse resolv.conf from %s: %w", src, err),
+		}
 	}
 	if _, ok := rc.Option("ndots"); ok {
 		rc.md.NDotsFrom = "host"
diff --git a/daemon/libnetwork/internal/resolvconf/resolvconf_test.go b/daemon/libnetwork/internal/resolvconf/resolvconf_test.go
index e1079653e4..8996e321c9 100644
--- a/daemon/libnetwork/internal/resolvconf/resolvconf_test.go
+++ b/daemon/libnetwork/internal/resolvconf/resolvconf_test.go
@@ -1,6 +1,7 @@
 package resolvconf
 
 import (
+	"bufio"
 	"bytes"
 	"io/fs"
 	"net/netip"
@@ -553,6 +554,16 @@ unrecognised thing
 	assert.Check(t, golden.String(string(content), t.Name()+".golden"))
 }
 
+// TestRCParseErrors tests that attempting to read a resolv.conf with a
+// very long line produces a useful error.
+// see https://github.com/moby/moby/issues/51679#issuecomment-3714403300
+func TestRCParseErrors(t *testing.T) {
+	input := strings.Repeat("a", bufio.MaxScanTokenSize+1) + "\n"
+
+	_, err := Parse(bytes.NewBufferString(input), "/etc/resolv.conf")
+	assert.Error(t, err, `failed to parse resolv.conf from /etc/resolv.conf: line too long (exceeds 65536)`)
+}
+
 func BenchmarkGenerate(b *testing.B) {
 	rc := &ResolvConf{
 		nameServers: []netip.Addr{