Sensory perception can modulate aging and physiology across taxa. We found that perception of female sexual pheromones through a specific gustatory receptor expressed in a subset of foreleg neurons in male fruit flies, Drosophila melanogaster, rapidly and reversibly decreases fat stores, reduces resistance to starvation, and limits life span. Neurons that express the reward-mediating neuropeptide F are also required for pheromone effects. High-throughput whole-genome RNA sequencing experiments revealed a set of molecular processes that were affected by the activity of the longevity circuit, thereby identifying new candidate cell-nonautonomous aging mechanisms. Mating reversed the effects of pheromone perception; therefore, life span may be modulated through the integrated action of sensory and reward circuits, and healthy aging may be compromised when the expectations defined by sensory perception are discordant with ensuing experience.