In family-living species, the quality and patterning of caregiving is the product of an individual's role within the family (mother, father, sibling) and parental experience, both of which interact with underlying neurobiological substrates. Among these substrates are the nonapeptides vasopressin and oxytocin, which modulate maternal, paternal, and alloparental care. We used a nonhuman primate model of the "nuclear family," the marmoset (Callithrix jacchus), to investigate relationships between caregiving experience, role within the family, and activation of either the oxytocin or vasopressin systems in shaping responsiveness to offspring. During two phases of offspring development (early infancy, juvenile), mothers, fathers, and older siblings were treated with vasopressin, oxytocin, or saline via intranasal application, and tested for responses to infant distress stimuli in a within-subjects design. Interest in infant stimuli was highest among marmosets that were caring for infants compared to those caring for juveniles, and parentally experienced marmosets were quicker to respond to infant stimuli than first-time caregivers. Moreover, marmosets treated with vasopressin showed enhanced responsiveness to infant stimuli compared to control stimuli only when caring for infants. Thus, in all classes of marmoset caregivers, vasopressin enhances responsiveness to infant-associated stimuli in caregivers during periods in which infant care is most crucial.