Reproductive success relies on the coordination of social behaviors, such as territory defense, courtship, and mating. Species with extreme variation in reproductive tactics are useful models for identifying the neural mechanisms underlying social behavior plasticity. The plainfin midshipman (Porichthys notatus) is a teleost fish with two male reproductive morphs that follow widely divergent developmental trajectories and display alternative reproductive tactics (ARTs). Type I males defend territories, court females, and provide paternal care, but will resort to cuckoldry if they cannot maintain a territory. Type II males reproduce only through cuckoldry. We sought to disentangle gene expression patterns underlying behavioral tactic, in this case ARTs, from those solely reflective of developmental morph. Using RNA-sequencing, we investigated differential transcript expression in the preoptic area-anterior hypothalamus (POA-AH) of courting type I males, cuckolding type I males, and cuckolding type II males. Unexpectedly, POA-AH differential expression was more strongly coupled to behavioral tactic than morph. This included a suite of transcripts implicated in hormonal regulation of vertebrate social behavior. Our results reveal that divergent expression patterns in a conserved neuroendocrine center known to regulate social-reproductive behaviors across vertebrate lineages may be uncoupled from developmental history to enable plasticity in the performance of reproductive tactics.