<p>Conspecific individuals can benefit from behavioral interactions, but whether cooperative behaviors require dedicated control in the nervous system is poorly understood. We examine the genetics underlying obligate cooperative male behaviors in honeybee colonies (<i>Apis mellifera</i>) that are deeply hardwired. We screened for transcription factor genes and found that only the <i>fruitless</i> (<i>fru</i>) BTB zinc-finger gene was restricted to expression in males and in the nervous system. Reporter coexpression revealed Fru-positive neuronal cell populations that are involved in processing and integrating sensory information. Computer-assisted behavioral tracking of male bees with loss-of-function mutations in experimental colonies revealed that <i>fru</i> is specifically required for the rate and/or duration of social approach and feeding behaviors, suggesting that the gene scales bees’ participation in the collective nutrition task. Together, our study establishes a gene-based specification of behavior initiation and sustainment and provides insight into the connection between cooperation and defined neural populations.</p>