Mating and aggression are innate social behaviors that are controlled by subcortical circuits in the extended amygdala and hypothalamus [1][2][3][4] . The bed nucleus of the stria terminalis (BNSTpr) is a node that receives input encoding sex-specific olfactory cues from the medial amygdala (MeApd) 5,6 , and which in turn projects to hypothalamic nuclei that control mating 7-9 (MPOA) and aggression 9-14 (VMHvl), respectively 15 . Previous studies have demonstrated that male aromatase + BNSTpr (AB) neurons are required for mounting and attack, and may identify conspecific sex according to their overall level of activity 16 . However neural representations in BNSTpr, their function and their transformations in the hypothalamus have not been characterized. Here we have performed calcium imaging 17,18 of male BNSTpr Esr1 neurons during social behaviors. We identify distinct populations of female-vs. male-tuned neurons in BNSTpr, with the former outnumbering the latter by ~2:1, similar to MeApd and MPOA but opposite to VMHvl, where male-tuned neurons predominate 6,9,19 . Chemogenetic silencing of BNSTpr Esr1 neurons whilst imaging MPOA Esr1 or VMHvl Esr1 neurons in behaving animals revealed, unexpectedly, that the male-dominant sex-tuning bias in VMHvl was inverted to female-dominant, while a switch from sniff-to mount-selective neurons during mating was attenuated in MPOA. Our data also indicate that BNSTpr Esr1 neurons are not essential for conspecific sex identification. Rather, they control the transition from appetitive to consummatory phases of male social behaviors by shaping sexand behavior-specific neural representations in the hypothalamus.