Triepeolus Robertson (Hymenoptera: Apidae: Nomadinae) is the second-largest genus of cleptoparasitic apid bees in the world but its evolutionary diversification through space and time has not been previously investigated. We present a dated phylogeny based on ultraconserved elements that includes 64 Triepeolus and 21 representative species of all seven other genera in the tribe Epeolini and propose a subgeneric classification for Triepeolus and its sister genus, Epeolus Latreille. Argyroselenis Robertson stat. rev., Pyrrhomelecta Ashmead stat. rev. and Trophocleptria Holmberg stat. rev. are removed from synonymy with Epeolus and recognized as valid subgenera. Three new subgenera are proposed for Epeolus—Ectopodus Onuferko subgen. nov., Gongronotus Onuferko subgen. nov. and Worfapis Onuferko subgen. nov.—and another three for Triepeolus: Placopyge Onuferko subgen. nov., Pseudodoeringiella Onuferko subgen. nov. and Rightmyera Onuferko subgen. nov. The subtribes Rhogepeolina syn. nov. and Thalestriina syn. nov. are synonymized under Odyneropsina and Epeolina, respectively. Divergence dating analysis inferred that Epeolus and Triepeolus originated sometime between the early Oligocene and early Miocene. Whereas the other epeoline genera most likely originated within the Neotropics, Epeolus and Triepeolus most likely originated within the Holarctic region, with the Bering Land Bridge identified as the route by which epeolines reached the Old World. Although Triepeolus diversity predictably reflects that of its main host taxon—long-horned bees (Hymenoptera: Apidae: Eucerinae)—the evolutionary mechanisms by which Triepeolus was able to diversify into the largest genus in its tribe are not yet clear and require further investigation.