Steroid-sensitive vasopressin (AVP) neurons in the bed nucleus of the stria terminalis (BNST) and medial amygdala (MeA) have been implicated in the control of social behavior, but the connectional architecture of these cells is not well understood. Here we used a modified rabies virus (RV) approach to identify cells that provide monosynaptic input to BNST and MeA AVP cells, and an adeno-associated viral (AAV) anterograde tracer strategy to map the outputs of these cells. Although the location of in- and outputs of these cells generally overlap, we observed several sex differences with differences in density of outputs typically favoring males, but the direction of sex differences in inputs vary based on their location. Moreover, the AVP cells located in both the BNST and MeA are in direct contact with each other suggesting that AVP cells in these two regions act in a coordinated manner, and possibly differently by sex. This study represents the first comprehensive mapping of the sexually dimorphic and steroid-sensitive AVP neurons in the mouse brain.