Dysregulation in the vasopressinergic system has been linked to social behavior deficits and Autism in humans. We utilized Shank3B+/- mice, a murine ASD model, to examine social behavior abnormalities associated with the pathology. Our findings not only confirmed well-documented sociability deficit, but also revealed a reduction in social aggression. We hypothesized that a dysregulated vasopressinergic system might contribute to the observed impairments in social behavior. The lateral septum (LS), a brain region implicated in social behaviors and densely innervated with arginine vasopressin (AVP) fibers, emerged as a potential key player. We identified a decrease in AVP+ somas in the bed nucleus of the stria terminalis (BNST), resulting in reduced AVP+ fiber density in the LS. Silencing these cells in Avp-Cre mice impaired sociability and social aggression. Using fiberphotometry, we demonstrated that BNST AVP+ projections to the LS were activated during sociability and aggression, with heightened activity during social aggression. Optogenetic silencing of these terminals also led to deficits in sociability and social aggression. Further investigation revealed that these impairments were mediated by the peptide release, as Cre-dependent shRNA virus injection in the BNST caused similar deficits. Rescuing sociability in Shank3B+/- mice was achieved by infusing an agonist of the vasopressin receptor 1a (Avpr1a) directly into the LS, without increasing aggression. Conversely, the agonist of the vasopressin receptor 1b (Avpr1b) promoted aggression without rescuing sociability. These findings unveil the selective modulation of diverse behaviors through distinct receptors within the same circuit, providing valuable insights for translational applications in ASD treatment.