The adult brain can flexibly adapt behaviors to specific life-stage demands. For example, while sexually naïve male mice are aggressive to the conspecific infants, father mice provide caregiving to them. How this behavioral shift from infanticidal to parental state is implemented at the level of neural circuits remains poorly understood. Vasopressin is a neural hormone produced in the paraventricular nucleus of the hypothalamus. We herein show that vasopressin suppresses pup-directed aggression in male mice. Vasopressin is known to activate oxytocin receptors (OTRs) as well as its canonical receptors, a phenomenon called ligand-receptor crosstalk. We found that vasopressin-mediated suppression of aggression is impaired by pharmacological blockage of OTRs or conditional knockout of the OTR gene from the preoptic regions, suggesting that vasopressin-to-OTR signaling contributes to the inhibition of pup-directed aggression. The chemogenetic activation of OTR+ neurons in the preoptic regions is sufficient to induce paternal caregiving behaviors. Collectively, our study demonstrates that vasopressin-derived suppression of aggression is, in part, mediated via OTR signaling in preoptic regions. This is, to our knowledge, the first in vivo functional characterization of non-canonical vasopressin-to-OTR crosstalk.