Central vasopressin pathways have been implicated in the mediation of paternal behavior, selective aggression, and affiliation in monogamous prairie voles. Here we demonstrate markedly different patterns of brain vasopressin receptor binding in the monogamous prairie vole and the congeneric nonmonogamous (promiscuous) montane vole. Vasopressin binding was assessed with both 3H-vasopressin and 125I-sarc-AVP using receptor autoradiography. The specificity of binding was consistent with a V1a receptor, the saturation kinetics were similar in the two species, and neither species showed evidence of sexual dimorphisms. In the prairie vole, highest specific binding was observed in the accessory olfactory bulb, diagonal band, laterodorsal thalamus, and superior colliculus. In the montane vole, specific binding was observed in the accessory olfactory bulb and superior colliculus as well, but in several other regions with high levels of binding in the prairie vole, binding was low or undetectable in the montane vole. In this nonmonogamous species, specific binding was high in lateral septum. Functional studies demonstrated the induction of phosphoinositol by AVP in the septum of the montane vole but not in the prairie vole. The pattern of 125I-sarc-AVP binding to lateral septum may reflect the social organization of these two species, as similar differences in AVP receptor distribution in the lateral septum were also observed in two related species, pine voles and meadow voles, which are monogamous and nonmonogamous, respectively. These results, along with earlier studies of AVP's effects on pair bonding, suggest the importance of this neuropeptide for the mediation of behaviors related to social organization.