ABSTRACT This is the fourth contribution within an ongoing series dedicated to the phylogeny and taxonomy of powdery mildews. This particular installment undertakes a comprehensive evaluation of a group previously referred to as the “Uncinula lineage” within Erysiphe. The genus Erysiphe is too large to be assessed in a single paper; thus, the treatment of Erysiphe is split into three parts, according to phylogenetic lineages. The first paper, presented here, discusses the most basal lineage of Erysiphe and its relationship to allied basal genera within tribe Erysipheae (i.e., Brasiliomyces and Salmonomyces). ITS+28S analyses are insufficient to resolve the basal assemblage of taxa within the Erysipheae. Therefore, phylogenetic multilocus examinations have been carried out to better understand the evolution of these taxa. The results of our analyses favor maintaining Brasiliomyces, Bulbomicroidium, and Salmonomyces as separate genera, at least for the interim, until further phylogenetic multilocus data are available for additional basal taxa within the Erysipheae. The current analyses also confirmed previous results that showed that the “Uncinula lineage” is not exclusively composed of Erysiphe species of sect. Uncinula but also includes some species that morphologically align with sect. Erysiphe, as well as species that had previously been assigned to Californiomyces and Typhulochaeta. Numerous sequences of Erysiphe species from the “Uncinula lineage” have been included in the present phylogenetic analyses and were confirmed by their position in well-supported species clades. Several species have been sequenced for the first time, including Erysiphe clintonii, E. couchii, E. geniculata, E. macrospora, and E. parvula. Ex-type sequences are provided for 16 taxa including E. nothofagi, E. trinae, and E. variabilis. Epitypes are designated and ex-epitype sequences are added for 18 taxa including Erysiphe carpophila, E. densa, and U. geniculata var. carpinicola. The new species Erysiphe canariensis is described, and the new names E. hosagoudarii and E. pseudoprunastri and the new combination E. ampelopsidis are introduced.