The neuropeptides arginine vasopressin (AVP) and oxytocin (OT) are key modulators of vertebrate sociality. Although some general behavioral functions of AVP and OT are broadly conserved, the detailed consequences of peptide release seem to be regulated by species-specific patterns of receptor distribution. We used autoradiography to characterize central vasopressin 1a receptor (V1aR) and OT receptor (OTR) distributions in two species of singing mice, ecologically specialized Central American rodents with a highly developed form of vocal communication. While both species exhibited high V1aR binding in the auditory thalamus (medial geniculate), binding in structures involved in vocal production (periaqueductal gray and anterior hypothalamus) was significantly higher in the more vocal species, Scotinomys teguina. In S. xerampelinus, receptor binding was significantly higher in a suite of interconnected structures implicated in social and spatial memory, including OTR in the hippocampus and medial amygdala, and V1aR in the anterior and laterodorsal thalamus. This pattern is concordant with species differences in population density and social spacing, which should favor enhanced sociospatial memory in S. xerampelinus. We propose that V1aR and OTR distributions in singing mice support an integral role for the AVP/OT system in several aspects of sociality, including vocal communication and sociospatial memory.