The genus Otarion Zenker, 1833, first appears in the Wenlock simultaneously with Cyphaspis Burmeister, 1843, as the oldest known species of each occur together in the southern Mackenzie Mountains of the Canadian Northwest Territories. The genera are unambiguous sister groups, a relationship supported most compellingly by a uniquely derived and distinctive pattern of juvenile cephalic spines, shared also with the Carboniferous genus Namuropyge Richter and Richter, 1939. This sister group relationship permits the development of a robust and stratigraphically correlated hypothesis of relationship among the adequately known species of Otarion, Otarion, Cyphaspis, and Namuropyge constitute the tribe Otarionini. The Mississippian genus Dixiphopyge Brezinski, 1988, may also belong to Otarionini. Namuropyge is a paedomorph, likely derived from a Degree Six or Seven meraspid of an older species of uncertain position in the Otarion–Cyphaspis clade.Three Wenlock species of Otarion occur in stratigraphic succession in a single section in the Mackenzie Mountains. Analysis of morphological change with time, and of sequential ontogenies, suggests that the Silurian history of the genus was dominated by incidents of peramorphosis.New species are Otarion huddyi, O. beukeboomi, and O. coppinsensis. Otarion brauni Perry and Chatterton, 1979, is revised.