show Abstracthide AbstractMicrobiomes make up as much as 90% of cells and 99% of unique genes in their hosts. The microbiome impacts a variety of processes including a host's ability to access nutrients and maintain health. While species differences in microbiomes have been described across ecosystems, little is known about how microbiomes of individual hosts assemble, particularly in the ecological and social contexts in which they evolved. We examined gut microbiome assembly within nine sympatric wild non-human primate (NHP) species in a community in which a strong hunter-prey relationship exists between chimpanzees (Pan troglodytes verus) and colobines. Despite sharing a common environment, and regular interspecific interactions, we found that individuals harbored unique and persistent microbiomes that were influenced by host species, social group, and parentage, but not social relationships among members of the same social group. We found a branching order of host-species networks constructed using the composition of their microbial communities as characters, which was incongruent with known NHP phylogenetic relationships, with chimpanzees sister to their colobine prey. In contrast to strong evidence of phylogenetic clustering in the microbiomes of all monkeys, chimpanzee microbiomes showed phylogenetic overdispersion. We suggest this reflects unique ecological processes driving microbiome assembly in chimpanzees, possibly due to broader exposure through hunting and microbiome assimilation of their primate prey. Our comprehensive study of contemporaneous microbiomes of all sympatric diurnal NHP in an ecosystem highlights the diverse transmission routes that shape these complex communities.