<p>Gene duplication and loss play an important role in the evolution of the major histocompatibility complex (MHC). Variations in copy number and sequence diversity of MHC genes can have significant fitness consequences. Here, we characterized both MHC class I and class II genes in a group of parrots—lovebirds (<i>Agapornis</i> spp.) using cloning and sequencing, quantitative PCR, and depth-of-coverage (DoC) analysis with whole-genome re-sequencing data. We identified copy number variation in MHC class II genes, with <i>A. roseicollis</i> having a single MHCIIB gene copy, whereas <i>A. canus</i> possesses at least three gene copies. Conversely, the copy number of class I genes is invariable, with only one copy identified in each <i>Agapornis</i> species. Phylogenetic reconstructions revealed both concerted evolution and trans-species polymorphism of MHC genes. In both MHC class I and II genes, sequences from the recently diverged eye-ringed species (e.g., <i>A. fischeri</i>, <i>A. personatus</i>, and <i>A. nigrigenis</i>) and their sister species <i>A. roseicollis</i> showed an intercalating pattern with no species-specific clustering, consistent with trans-species polymorphism. In contrast, sequences from the early-diverged species (e.g., <i>A. canus</i> and <i>A. pullarius</i>) clustered by species, which is typical for avian MHC genes undergoing concerted evolution. The pattern of MHC copy number variation and modes of evolution observed are associated with the timescale of species divergence. We suggest that future studies should include both MHC class I and II genes and multiple species spanning a range of divergence time to enhance our understanding of the evolution of avian MHC diversity.</p>