Microbiomes impact a variety of processes including a host’s ability to access nutrients and maintain health. While host species differences in microbiomes have been described across ecosystems, little is known about how microbiomes assemble, particularly in the ecological and social contexts in which they evolved. We examined gut microbiome composition in nine sympatric wild non-human primate (NHP) species. Despite sharing an environment and interspecific interactions, individuals harbored unique and persistent microbiomes influenced by host species, social group, and parentage, but surprisingly not by social relationships among members of a social group. We found a branching order of host-species networks constructed using the composition of their microbiomes as characters, which was incongruent with known NHP phylogenetic relationships, with chimpanzees (Pan troglodytes verus) sister to colobines, upon which they regularly prey. In contrast to phylogenetic clustering found in all monkey microbiomes, chimpanzee microbiomes were unique in that they exhibited patterns of phylogenetic overdispersion. This reflects unique ecological processes impacting microbiome composition in chimpanzees and future studies will elucidate the aspects of chimpanzee ecology, life history, and physiology that explain their unique microbiome community structure. Our study of contemporaneous microbiomes of all sympatric diurnal NHP in an ecosystem highlights the diverse dispersal routes shaping these complex communities. © 2018, International Society for Microbial Ecology.