AbstractThe organization of the body cavities is an important morphological trait that can be used for establishing the phylogenetic relationships between different groups of animals. In the present study, the hemocoel and coelomic systems of 10‐hr‐old juveniles and adults of the hermaphroditic oikopleurid Oikopleura gracilis were examined using light and transmission electron microscopy. The trunk hemocoel in 10‐hr‐old juveniles was represented by small clefts containing layers of extracellular matrix of adjacent tissues or interstices with migrating primordial germ syncytium. The wide hemocoel in the tail contained extracellular strands, subdividing the hemocoel into hemal sinuses. In adults, a large hemocoel appeared in the trunk and tail, and also contained extracellular strands. The hermaphroditic gonad was surrounded by its own lining, separating it from the hemocoel. The gamete‐filled cavity in the ovary and testis appeared only at late‐stage gonadogenesis, when the pre‐spawning reduction of syncytium occurred in the gonads. The true coelom in 10‐hr‐old juveniles and adults was represented by the pericardium. The lining of the pericardium consisted of myoepithelial and peritoneal cells. In the myoepithelial cells of 10‐hr‐old juveniles, myofibrils had been formed. The myoepithelial cells of adults had several parallel rows of completely differentiated myofibrils. The substantial reduction of the coelomic and circulatory systems in O. gracilis evidently results from the extreme shortening of ontogeny in appendicularians. Development in O. gracilis from early juvenile to adult involves the following steps, which also suggest how the tunicate heart may have evolved: a single‐layered coelomic sac gives rise to a grooved pericardium with an open hemal sinus (simple heart). In ascidians, this simple heart in turn gives rise to a closed tubular, double‐layered heart–pericardial complex, with a separate pericardial cavity and a closed heart, whose wall is formed by specialized myocardium.