Phylogenetic analyses within Poaceae tribe Poeae subtribes Puccinellinae (=Coleanthinae), Phleinae, Poinae s.l. (including Alopecurinae), and Miliinae (PPAM clade), revealed that one species formerly placed in Poa represents a new monotypic genus belonging to subtribe Poinae s.l., Dupontiopsis gen. nov., D. hayachinensis comb. nov. (based on Poa hayachinensis), endemic to wet, gravelly, serpentine, alpine habitats in northern Japan. This genus forms a strongly supported clade (DAD) with two circumarctic Poinae genera, Arctophila and Dupontia, in phylogenetic analyses of plastid and nuclear ribosomal DNA sequence data. Both morphology and DNA sequence analyses provide support for D. hayachinensis as a lineage distinct from either Arctophila or Dupontia, with moderate DNA support for a position as sister to these two genera. Dupontiopsis resembles these other monotypic genera in its several‐flowered spikelets, lemmas usually 3‐nerved, with frequently awned attenuate scarious apices (as in Dupontia) and calluses with a crown of hairs around the base of the lemma, but differs in its keeled lemmas, scabrous palea keels, glumes shorter than the first lemma. Our investigation suggests that the most recent shared ancestor of the DAD clade evolved from a single hybridization event, as a hexaploid, probably in western Beringia. The probable parentage of the ancestor is considered to be within the Poinae–Alopecurinae clade excluding Poa. We provide evidence for possible secondary hybridization and introgression of duodecaploid Dupontia fisheri with Puccinellia. A key to perennial genera of PPAM with hairy calluses, and a supplemental table of morphological characters in the genera accepted in PPAM are provided.