In most eukaryotes, aerobic respiration requires interactions between autosomally encoded genes (Ninteract genes) and mitochondrial DNA, RNA, and protein. In species where females are philopatric, contrasting distributions of genetic variation in mitochondrial and nuclear genomes create variation in mitonuclear interactions that may be subject to natural selection. To test this expectation, we turned to a group with extreme female philopatry: the macaque monkeys. We examined four genomic data sets from (1) wild caught and (2) captive populations of rhesus macaque, which is the most widely distributed nonhuman primate, and (3) the stump-tailed macaque and (4) a subspecies of longtail macaque, both of whose mitochondrial DNA is introgressed from a highly diverged ancestor. We identified atypically long runs of homozygosity, low polymorphism, high differentiation, and/or rapid protein evolution associated with Ninteract genes compared with non-Ninteract genes. These metrics suggest a subset of Ninteract genes were independently subject to atypically pervasive natural selection in multiple species. These findings suggest that natural selection on mitonuclear interactions could have influenced several aspects of macaque societies including species diversity, ecological breadth, female-biased adult sex ratio and demography, sexual dimorphism, and mitonuclear phylogenomics.