The oxytocin receptor (OXTR) and its ligand, oxytocin (OXT), regulate reproductive physiology (i.e., parturition and lactation) and sociosexual behaviors. To define the essential functions of OXTR, we generated mice with a null mutation in the Oxtr gene (Oxtr^-/-) and compared them with OXT-deficient (Oxt^-/-) mice. Oxtr^-/- mice were viable and had no obvious deficits in fertility or reproductive behavior. Oxtr^-/- dams exhibited normal parturition but demonstrated defects in lactation and maternal nurturing. Infant Oxtr^-/- males emitted fewer ultrasonic vocalizations than wild-type littermates in response to social isolation. Adult Oxtr^-/- males also showed deficits in social discrimination and elevated aggressive behavior. Ligand Oxt^-/- males from Oxt^-/- dams, but not from Oxt^+/- dams, showed similar high levels of aggression. These data suggest a developmental role for the OXT/OXTR system in shaping adult aggressive behavior. Our studies demonstrate that OXTR plays a critical role in regulating several aspects of social behavior and may have important implications for developmental psychiatric disorders characterized by deficits in social behavior.