Sex pheromones are key social signals in most animals. In Drosophila a dedicated olfactory channel senses a male pheromone, cis-vaccenyl acetate (cVA) that promotes female courtship while repelling males. Here we show that flies use separate cVA processing streams to extract both qualitative and positional information. We find that cVA olfactory neurons are exquisitely sensitive to concentration differences in a 5 mm range around a male fly. Second order projection neurons (PNs) detect bi-antennal differences in cVA concentration, which can reliably encode the angular position of a male. We identify an active circuit mechanism increasing left-right response differences in PNs including an interneuron performing this function by providing contralateral inhibition. At the third layer of the circuit, we find neurons with distinct response properties and sensory integration motifs. One population is selectively tuned to an approaching male with speed dependent responses. A second population responds tonically to a male fly’s presence and controls female mating-decisions. A third population integrates a male taste cue with cVA, and only a simultaneous presentation of both signals promotes female mating via this pathway. Interestingly, neurons encoding speed, a positional feature, are sexually monomorphic and do not regulate sexual behavior, while neurons encoding qualitative features of male presence are sexually dimorphic and regulate female receptivity. Our results show that the olfactory system generates a range of complex percepts in discrete populations of central neurons that allow the expression of appropriate behaviors depending on context. Spatial coding is generated by integration of bilateral sensory information like the auditory system while separation of what and where pathways is reminiscent of the visual cortex.