In this study, the relationships of the cestode order Bothriocephalidea, parasites of marine and freshwater bony fish, were assessed using multi-gene molecular phylogenetic analyses. The dataset included 60 species, covering about 70% of currently recognised genera, a sample of bothriocephalidean biodiversity gathered through an intense 15-year effort. The order, while being monophyletic, includes three non-monophyletic and one monophyletic family. Bothriocephalidae is monophyletic and forms the most derived lineage of the order, comprising a single freshwater and several marine clades. Biogeographic patterns within the freshwater clade are indicative of past radiations having occurred in Africa and North America. The earliest diverging lineages of the order are formed of a paraphyletic Triaenophoridae. The Echinophallidae, consisting nearly exclusively of parasites of bathypelagic fish, was also resolved as paraphyletic to the inclusion of the Bothriocephalidae. Philobythoides sp., the only representative of the Philobythiidae, another family of parasites of bathypelagic fish, formed a sister group to the genus Eubothrium, the latter forming one of the lineages of the paraphyletic Triaenophoridae. Because of the weak statistical support for most of the basal nodes of the Triaenophoridae and Echinophallidae, as well as the lack of obvious morphological synapomorphies shared by taxa forming statistically supported lineages, the current family-level classification is provisionally retained, with the exception of the family Philobythiidae, which is now recognised as a synonym of the Triaenophoridae. In addition, Schyzocotyle Akhmerov, 1960 is resurrected to accommodate the veterinary important, invasive Asian fish tapeworm, S. acheilognathi (Yamaguti, 1934) n. comb. (syn. Bothriocephalus acheilognathi Yamaguti, 1934) and S. nayaruensis (Malhotra, 1983) n. comb. The genus is morphologically characterised by a wide, heart-shaped scolex with narrow and deep bothria.