In pair-living mammals, genetic monogamy is extremely rare. One possible reason is that in socially monogamous animals, mate choice can be severely constrained, increasing the risk of inbreeding or pairing with an incompatible or low-quality partner. To escape these constraints, individuals might engage in extra-pair copulations. Alternatively, inbreeding can be avoided by dispersal. However, little is known about the interactions between mating system, mate choice, and dispersal in pair-living mammals. Here we genotyped 41 wild individuals from 14 groups of coppery titi monkeys (Plecturocebus cupreus) in Peruvian Amazon using 18 microsatellite loci. Parentage analyses of 18 young revealed no cases of extra-pair paternity, indicating that the study population is mostly genetically monogamous. We did not find evidence for relatedness- or heterozygosity-based mate choice. Despite the lack of evidence for active inbreeding avoidance via mate choice, mating partners were on average not related. We further found that dispersal was not sex-biased, with both sexes dispersing opportunistically over varying distances. Our findings suggest that even opportunistic dispersal, as long as it is not constrained, can generate sufficient genetic diversity to prevent inbreeding. This, in turn, can render active inbreeding avoidance via mate choice and extra-pair copulations less necessary, helping to maintain genetic monogamy.