Male sexual behavior is innate and rewarding. Despite its centrality to reproduction, a molecularly specified neural circuit governing innate male sexual behavior and reward remains to be characterized. We have discovered a developmentally wired neural circuit necessary and sufficient for male mating. This circuit connects chemosensory input to BNSTpr neurons, which innervate POA neurons that project to centers regulating motor output and reward. Epistasis studies demonstrate that BNSTpr neurons are upstream of POA neurons, and BNSTpr-released substance P following mate recognition potentiates activation of POA neurons through Tacr1 to initiate mating. Experimental activation of POA neurons triggers mating, even in sexually satiated males, and it is rewarding, eliciting dopamine release and self-stimulation of these cells. Together, we have uncovered a neural circuit that governs the key aspects of innate male sexual behavior: motor displays, drive, and reward.