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Abstract: Adult ocean sunfish are the heaviest living teleosts. They have no axial musculature or caudal fin. Propulsion is by unpaired dorsal and anal fins; a pseudocaudal fin (‘clavus’) acts as a rudder. Despite common perception, young sunfish are active predators that swim quickly, beating their vertical fins in unison to generate lift‐based propulsion and attain cruising speeds similar to salmon and marlin. Here we show that the thick subcutaneous layer (or ‘capsule’), already known to provide positive buoyancy, is also crucial to locomotion. It provides two compartments, one for dorsal fin musculature and one for anal fin muscles, separated by a thick, fibrous, elastic horizontal septum that is bound to the capsule itself, the roof of the skull and the dorsal surface of the short vertebral column. The compartments are braced sagittally by bony haemal and neural spines. Both fins are powered by white muscles distributed laterally and red muscles located medially. The anal fin muscles are mostly aligned dorso‐ventrally and have origins on the septum and haemal spines. Dorsal fin muscles vary in orientation; many have origins on the capsule above the skull and run near‐horizontally and some bipennate muscles have origins on both capsule and septum. Such bipennate muscle arrangements have not been described previously in fishes. Fin muscles have hinged tendons that pass through capsular channels and radial cartilages to insertions on fin rays. The capsule is gelatinous (89.8% water) with a collagen and elastin meshwork. Greasy in texture, calculations indicate capsular buoyancy is partly provided by lipid. Capsule, septum and tendons provide elastic structures likely to enhance muscle action and support fast cruising. [ABSTRACT FROM AUTHOR]