Divergent steroid hormone profiles can shape the development of male versus female neural phenotypes, but whether they also determine differences in the short-term, neurophysiological patterning of behavior is unknown. We now show that steroid hormone-specific modulation of a vocal pattern generator (VPG) diverges between reproductive morphs in a teleost fish. Only type I male midshipman acoustically court females, whereas type II males steal fertilizations from type I males and, like females, generate only agonistic calls. The androgen 11-ketotestosterone (11kT), but not testosterone (T), rapidly (within 5 min) increases type I VPG output. As now shown, T, but not 11kT, rapidly increases VPG output in type II males and females, consistent with the predominant circulating androgen in type II males and females (T) versus type Is (11kT). Receptor and enzyme antagonists reveal an unexpected divergence in androgen- versus estrogen-dependent mechanisms in, respectively, type II males versus females. Cortisol, the main circulating glucocorticoid, also has divergent actions: suppressing versus increasing VPG output in, respectively, type II males and females versus type Is. In summary, rapid steroid action on VPG activity is uncoupled from gonadal phenotype (convergent between type II males and females), whereas the receptor-mediated mechanisms of androgen action are predicted by gonadal phenotype (both male morphs are sensitive to androgen receptor blockade, whereas females are not). A comparable mix of neuroendocrine traits may explain the widespread distribution of intrasexual behavioral phenotypes among teleosts and vertebrates in general. Moreover, the fundamental organization/activation principles that predict the steroid-dependent expression of “maleness” and “femaleness” may now include rapid steroid actions on the neurophysiological patterning of behavior.