Powdery mildew, caused by Erysiphe spp., on oak has been shown to have serious ecological consequences on Quercus hosts. Erysiphe alphitoides and E. quercicola are two of the most heavily studied and common powdery mildews known to occur on Quercus species. In recent years, these species have been noted throughout the world on a range of hosts within and outside the Quercus genus. Reports that E. alphitoides was absent in European herbaria before 1921 and the discovery of the holotype of E. alphitoides from 1911 in an American herbarium (FH) led to the current study in which we genetically analysed six specimens of E. alphitoides s. lat including, most importantly, the holotype of E. alphitoides from France collected in 1911. The results of our analyses revealed that: (1) The sequence of the E. alphitoides holotype falls within the E. quercicola clade, confirming that E. alphitoides did not spread to Europe until ~1921. (2) E. alphitoides var. chenii forms a monophyletic clade with E. epigena and should be reduced to synonymy with that species and (3) through sequence analyses E. alphitoides and E. quercicola are confirmed to have spread to North America. The sequencing results of the E. alphitoides holotype have severe nomenclatural-taxonomic consequences. A proposal was submitted simultaneously with the present manuscript to conserve the name E. alphitoides so that the traditional usage of the names E. alphitoides and E. quercicola could be maintained. The sequences obtained for the current study provide new insight into the taxonomy and spread of these ecologically significant, globally distributed species. The present study highlights the importance of sequencing specimens from type material, above all when morphological similar species are involved.