This study documents the development of inter- and intrasexual dimorphisms in the vocal ('sonic') muscles of the swimbladder in the plainfin midshipman fish, Porichthys notatus. Midshipman have two male reproductive morphs, Types I and II. Only Type I males build nests and generate mate calls to attract females; Type II males sneak or satellite spawn. Vocal muscles in the mate-calling Type I males were 25-fold larger in absolute size (sixfold larger when scaled to body size) compared with females or non-calling Type II males. Dimorphisms in muscle mass were correlated with dimorphisms in fiber number and diameter. Only nascent Type I males experienced a pre-maturational, fourfold increase of fiber number followed by a rapid, fivefold increase in fiber cross-sectional area at sexual maturity. Also specific to Type I males was a striking change in cell structure: the ratio of sarcoplasm to myofibril area increased fivefold. By contrast, Type II males and females matured without showing any of these changes in sonic muscle – the trajectories which described juvenile growth continued to hold through maturity and adulthood. The results indicate distinct, non-sequential, ontogenetic trajectories for Type I and Type II males. The origin of the Type II male morphotype is described as paedomorphosis by progenesis: size distributions of free-living animals suggest that Type II males can mature precocially as one-year-old fish, whereas Type I males defer reproduction until they are at least two years of age.