Grammitidoideae are the largest subfamily in Polypodiaceae and contain about 911 species. Progress has been made in understanding the overall phylogeny and generic boundaries in the light of recent molecular works. However, the majority of species, especially Asian species, and some critical type species of genera remain unsampled. In this study, a dataset of six plastid markers of 1003 (112 new) accessions representing ca. 412 species of Grammitidoideae including the type species of Ctenopterella, Grammitis, Moranopteris, Radiogrammitis, and Themelium, was assembled to infer a phylogeny. Our major results include: (1) the type species of Grammitis is successfully sequenced using a next‐generation sequencing technique and is resolved in Grammitis s.str. as expected; (2) Ctenopterella is found to be polyphyletic and a new clade consisting of C. khaoluangensis is resolved as sister to Tomophyllum; (3) the type species of Ctenopterella is resolved in a clade sister to the C. lasiostipes clade; (4) Oreogrammitis is found to be polyphyletic and three clades outside of the core Oreogrammitis are identified containing O. subevenosa and allies, O. orientalis, and O. beddomeana (+ O. cf. beddomeana); (5) Prosaptia is found to be paraphyletic with P. nutans being sister to a clade containing the rest of Prosaptia and Archigrammitis; (6) the intergeneric and major relationships within the Asia‐Pacific clade are well resolved and strongly supported except for a few branches; (7) extensive cryptic speciation is detected in the Asia‐Pacific clade; and (8) based on the polyphyly of Ctenopterella we describe three new genera, Boonkerdia, Oxygrammitis, and Rouhania, for species formerly in Ctenopterella; because the type species of Grammitis belongs to Grammitis s.str., we describe five new genera, Aenigmatogrammitis, Grammitastrum (stat. nov.), Howeogrammitis, Nanogrammitis, and Thalassogrammitis for species formerly in Grammitis s.l. A key to the 35 Old‐World genera is given, a taxonomic treatment is presented, and the morphology of all new genera is shown with either a color plate and/or a line drawing.