Contemporary theory on the role of oxytocin and vasopressin in mammalian social bonds has been shaped by seminal vole research that revealed interspecific variation in neuroendocrine circuitry by mating system. The Eulemur genus of strepsirrhine primates contains socially monogamous (MO) and non-monogamous (NM) species, making it the sole primate analog to Microtus, and offering a rare opportunity for comparative nonapeptide research with greater evolutionary relevance to humans. Relying on natural mortality, we performed oxytocin and arginine vasopressin 1a receptor (OXTR; AVPR1a) autoradiography on 12 Eulemur brains (4 MO; 8 NM), representing seven species, to characterize OXTR/AVPR1a distributions across species and compare variation in receptor distributions as a function of mating system. Consistent with the ‘intermediary’ phylogenetic placement of strepsirrhines, some OXTR/AVPR1a binding patterns were reminiscent of olfactory-guided rodents and others were congruent with more visually oriented haplorhines. By mating system, several nuclei showed differential receptor expression, potentially consistent with a role for both neuropeptides in monogamy, but most areas previously identified as part of a rodent ‘pair-bonding circuit’ did not exhibit comparable differential receptor expression in Eulemur. Circuits identified as key to pair-bonding in rodents cannot be directly invoked to explain pair-bonding in primates. Mapping neurocircuitry in non-model species informs evolutionary mechanisms and neurobiological bases underlying diversity in primate social systems, and studies in nonhuman primates may serve as a valuable bridge for translating findings in rodents to human biology and sociality. Funded by NSF.