Genes of the major histocompatibility complex (MHC) are essential in vertebrate adaptive immunity, and they are highly diverse and duplicated in many lineages. While it is widely established that pathogen-mediated selection maintains MHC diversity through balancing selection, the role of mate choice in shaping MHC diversity is debated. Here, we investigate female mating preferences for MHC class II (MHCII) in the bluethroat (Luscinia svecica), a passerine bird with high levels of extra-pair paternity and extremely duplicated MHCII. We genotyped family samples with mixed paternity and categorized their MHCII alleles according to their functional properties in peptide binding. Our results strongly indicate that females select extra-pair males in a non-random, self-matching manner that provides offspring with an allelic repertoire size closer to the population mean, as compared to offspring sired by the social male. This is consistent with a “compatible genes” model for extra-pair mate choice where the optimal allelic diversity is intermediate, not maximal. This “golden mean” presumably reflects a trade-off between maximizing pathogen recognition benefits and minimizing autoimmunity costs. Our study exemplifies how mate choice can reduce the population variance in individual MHC diversity and exert strong stabilizing selection on the trait. It also supports the hypothesis that extra-pair mating is adaptive through enhanced genetic quality of offspring.