ABSTRACT Erysiphe species infecting oaks in North America are common and widespread, but compared to Asia and Europe, the taxonomy and phylogeny of North American species is unknown. The present study addresses this dispairity. Comprehensive multilocus phylogenetic analyses, including CAM , GAPDH , GS , ITS, RPB2 and TUB , revealed a high degree of co‐evolution between North American oaks and the Erysiphe spp. that infect them. A concatenated multilocus tree and individual trees based on single loci revealed many highly supported species clades. The clades are formally named to conform with the current taxonomic classification. Available names, such as E. abbreviata , E. calocladophora and E. extensa , are associated with corresponding clades, and are newly circumscribed supported by ex‐type sequences or, if not available, by the designation of epitypes with ex‐epitype sequences. Erysiphe densissima is reintroduced for a clade that corresponds to the old name ‘ E. extensa var. curta’ . Eight new species are described, including Erysiphe carolinensis , E. gambelii , E. occidentalis , E. phellos , E. pseudoextensa , E. quercophila, E. quercus ‐laurifoliae and E. schweinitziana . A new diagnostically and taxonomically relevant trait associated with the anamorphs of North American Erysiphe species on oaks has been assssed. This is a special conidiophore‐like lateral outgrowth of the superficial hyphae, comparable to ‘aerial hyphae,’ which are also known for species of the powdery mildew genus Cystotheca which also infect Quercus species.