Although it is well appreciated that the early-life social environment asserts subsequent long-term consequences on offspring brain and behavior, the specific mechanisms that account for this relationship remain poorly understood. Using a novel assay that forced biparental pairs or single mothers to prioritize caring for offspring or themselves, we investigated the impact of parental variation on adult expression of nonapeptide-modulated behaviors in prairie voles. We demonstrated that single mothers compensate for the lack of a co-parent. Moreover, mothers choose to invest in offspring over themselves when faced with a tradeoff, whereas fathers choose to invest in themselves. Furthermore, our study suggests a pathway whereby variation in parental behavior (specifically paternal care) may lead to alterations in DNA methylation within the vasopressin receptor 1a gene and gene expression in the lateral septum. These differences are concomitant with changes in social approach, a behavior closely associated with septal vasopressin receptor function.