Background: In the arms race between hosts and parasites, genes involved in the immune response are targets for natural selection. Toll-Like Receptor (TLR) genes play a role in parasite detection as part of the innate immune system whereas Major Histocompatibility Complex (MHC) genes encode proteins that display antigens as part of the vertebrate adaptive immune system. Thus, both gene families are under selection pressure from pathogens. The bananaquit (Coereba flaveola) is a passerine bird that is a common host of avian malarial parasites (Plasmodium sp. and Haemoproteus sp.). We assessed molecular variation of TLR and MHC genes in a wild population of bananaquits and identified allelic associations with resistance/susceptibility to parasitic infection to address hypotheses of avian immune response to haemosporidian parasites. Results: We found that allele frequencies are associated with infection status at the immune loci studied. A consistent general trend showed the infected groups possessed more alleles at lower frequencies, and exhibited unique alleles, compared to the uninfected group. Conclusions: Our results support the theory of natural selection favoring particular alleles for resistance while maintaining overall genetic diversity in the population, a mechanism which has been demonstrated in some systems in MHC previously but understudied in TLRs.