Background: The gut microbiome (GM) can influence many biological processes in the host, impacting its health and survival, but the GM can also be influenced by the host’s traits. In vertebrates, Major Histocompatibility Complex (MHC) genes play a pivotal role in combatting pathogens and are thought to shape the host’s GM. However, despite this - and the documented importance of both GM and MHC variation to individual fitness - few studies have investigated the association between the GM and MHC in the wild. Results: We characterised MHC class I (MHC-I), MHC class II (MHC-II), and GM variation in individuals within a natural population of the Seychelles warbler, Acrocephalus sechellensis. We determined how the diversity and composition of the GM varied with MHC characteristics, in addition to environmental factors and other host intrinsic traits. Our results show that the presence of specific MHC alleles, but not MHC diversity, influences both the diversity and composition of the GM in this population. We found that MHC-I alleles, rather than MHC-II alleles, had the greatest impact on the GM. GM diversity was negatively associated with the presence of three MHC-I alleles (Ase-ua3, Ase-ua4, Ase-ua5), and one MHC-II allele (Ase-dab4), while changes in GM composition were associated with the presence of four different MHC-I alleles (Ase-ua1, Ase-ua7, Ase-ua10, Ase-ua11). GM diversity was also positively correlated with genome-wide heterozygosity and varied with host age and field period.Conclusions: These results suggest that components of the host’s immune system play a role in shaping the GM of wild animals. Host genotype – specifically, adaptive immune receptor MHC-I alleles – can modulate the GM, although whether this occurs directly, or indirectly through effects on host health is unclear. To our knowledge this is the first-time individual MHC-I variation has been shown to be associated with differences in GM characteristics in a natural population. Importantly, it suggests that host–microbiome coevolution may play a role in maintaining functional immunogenetic variation within natural vertebrate populations.