Genes of the major histocompatibility complex (MHC) are a critical part of the adaptive immune response, and the most polymorphic genes in the vertebrate genome, especially in passerine birds. This diversity is thought to be influenced by exposure to pathogens which can vary in relation to numerous factors. Migratory behaviour may be a particularly important trait to consider because migratory birds are exposed to a greater number of different pathogens and parasites at both breeding (i.e. temperate) and overwintering (i.e. tropical and subtropical) areas, as well as at stopover sites during migration. Thus, migrants are predicted to have greater MHC diversity than residents. We compared MHC variation, at both class I and II, and levels of haemosporidian infection between one resident and two migratory populations of the common yellowthroat (Geothlypis trichas). We found that residents were less likely to be infected with haemosporidian parasites and had lower MHC diversity at class I; however, variation at MHC class II was greater in residents than migrants, contrary to our prediction. These patterns were not likely to be caused by differences in population demography as genome-wide heterozygosity (based on 9225 single-nucleotide polymorphisms) was high in all three populations and not correlated with MHC variation. Our different results for MHC class I and II suggest that studies of immune gene variation in relation to life history need to consider that there could be different selection pressures arising from intracellular (class I) and extracellular (class II) pathogens in different populations.