Abstract The roughly 500 species of cheilanthoid ferns exhibit a diversity of morphological adaptations to xeric environments. However, most of these traits have evolved independently multiple times, impeding past efforts to establish a natural classification for the group. Considerable progress has been made over the past three decades resolving most of the major lineages, with the notable exception of the hemionitids, the largest and most widely distributed clade. The nearly 350 hemionitid species can be found in dry regions across the globe and account for two‐thirds of cheilanthoid diversity. While some of the 17 genera commonly attributed to this group are easily recognized and demonstrably monophyletic, others have been shown to be clearly non‐monophyletic. Here, we explore phylogenetic relationships among hemionitid species using a dataset that greatly expands on earlier studies. We carefully consider generic lines and propose a phylogenetically informed classification that better aligns with morphology, geography, and evolutionary history. Based on our analyses and morphological investigations, we propose the recognition of 22 monophyletic hemionitid genera. Nine of our generic circumscriptions are consistent with those of most other recent studies. Two other genera are expanded relative to these studies, while two are more narrowly defined. Two generic names are resurrected herein and seven genera are newly described to accommodate divergent clades. In all, 106 new species‐level (plus 9 subspecific) combinations are made.