Human activities can cause habitat degradation that may alter the types and quality of available food resources and thus influence the microbiomes of wild animal populations. Furthermore, seasonal shifts in food availability may cause adaptive responses in the gut microbiome to meet the need for different metabolic capabilities. Here, we demonstrate local-scale population structure in the gastrointestinal microbiotas of Chlorocebus monkeys, in southern Ethiopia, in response to varying degrees of human encroachment. We further provide evidence of adaptation to ecological conditions associated with the dry and wet seasons, and show seasonal effects to be more pronounced in areas with limited human activity. Finally, we report species-level microbiota differences between the endemic Ethiopian Bale monkey, an ecological specialist, and generalist Chlorocebus species from the same geographical region.