Passerine birds belong to the most species rich bird order and are found in a wide range of habitats. The extremely polymorphic adaptive immune system of passerines, identified through their major histocompatibility complex class I genes (MHC-I), may explain some of this extreme radiation. Recent work has shown that passerines have higher numbers of MHC-I gene copies than other birds, but little is currently known about expression and function of these gene copies. Non-passerine birds have a single highly expressed MHC-I gene copy, a pattern that seems unlikely in passerines. We used high-throughput sequencing to study MHC-I alleles in siskins (Spinus spinus) and determined gene expression, phylogenetic relationships and sequence divergence. We verified between six and 16 MHC-I alleles per individual and 97% of these were expressed. Strikingly, up to five alleles per individual had high expression. Out of 88 alleles 18 were putatively non-classical with low sequence divergence and expression, and found in a single phylogenetic cluster. The remaining 70 alleles were classical, with high sequence divergence and variable degrees of expression. Our results contradict the suggestion that birds only have a single dominantly expressed MHC-I gene by demonstrating several highly expressed MHC-I gene copies in a passerine.