Parental care is critical to offspring survival, yet we know little about how genetic differences affect the brain to modify parental care. Using a monogamous and a promiscuous species of deer mice (genus Peromyscus), which we show have large differences in parental behaviour, we perform a genetic screen to identify loci that affect parental care. We find that some loci have a specific effect on single parental traits whereas other loci affect modules of traits; moreover, some loci act in a sex-specific manner whereas others have similar effects in both sexes. Importantly, we also drilled down into one locus associated with parental nest building that contains the vasopressin gene and find that vasopressin is expressed at higher levels in the hypothalamus of the promiscuous species, which builds less sophisticated nests. Using chemogenetic studies in laboratory mice, we demonstrate that exciting or repressing vasopressin neurons can suppress or promote nest building, respectively. Together, our genetic dissection of parental behaviour opens exciting new avenues of research for the neurobiological understanding of complex social behaviour such as parenting.