Collection of new material from the bamboosharks Chiloscyllium indicum (Gmelin, 1789) and Chiloscyllium hasseltii Bleeker, 1852, from Indonesian and Malaysian Borneo prompted reevalutation of the identity and host associations of the cestode genus Carpobothrium Shipley and Hornell, 1906. Light microscopical examination of whole mounts, histological sections, and egg preparations, in combination with scanning electron microscopy of scoleces, led to redescription of the type species Carpobothrium chiloscyllii Shipley and Hornell, 1906, from Ch. indicum, as well as description of a new species from Ch. hasseltii. The proglottid anatomy of C. chiloscyllii is described for the first time. The genus was confirmed to exhibit pouch-like bothridia with relatively small anterior and posterior flaps that have a tendency to retract into the bothridial pouches, testes that are entirely pre‐poral, a uterus that extends only to the cirrus sac, and a vas deferens that coils posterior to the cirrus sac. Although not previously reported for the genus, both species were determined to possess an apical sucker on the anterior margin of the anterior bothridial flap. The posterior coiling of the vas deferens allowed free gravid proglottids of the new Carpobothrium species to be distinguished from those of Yorkeria Southwell, 1927, and to determine that, while eggs of the former are spherical with bipolar filaments, those of the latter are spindle-shaped with unipolar filaments. Examination of some of Southwell’s material identified as C. chiloscyllii from the batoid hosts Urogymnus asperrimus Bloch and Schneider, 1801 and Rhynchobatus djeddensis Forsskål, 1775, in Sri Lanka, confirmed evidence from molecular work suggesting that these cestodes, which also bear pouch-like bothridia, represent a distinct group of cestodes from those parasitizing bamboosharks. This work both confirms the association of Carpobothrium species with sharks of the genus Chiloscyllium Müller and Henle, 1837, and paves the way for establishment of a novel genus for the taxa parasitizing batoids.