To understand the phylogenetic relationships and evolution of the powdery mildew genus Sawadaea (Ascomycota: Erysiphaceae), obligate parasitic fungi of maples, we performed molecular phylogenetic analyses based on 47 ITS and ten 28S rDNA sequences. Seven major clades of Sawadaea, each represented by powdery mildew specimens collected from a single or a small number of closely related sections of Acer (maples), were identified in this study, suggesting that a close evolutionary relationship exists between Acer (host) and Sawadaea (parasite). A 6–11-base insertion/deletion was found in the ITS1 region of Sawadaea, and the presence or absence of the indel was consistent within the respective clades. Because the outgroup genera Podosphaera and Cystotheca have no deletions in these sites, deletion of the sequences may have occurred during the divergence of the respective clades of Sawadaea. The seven clades of Sawadaea were divided into two geographical groups, viz. an East Asian and a global group, based on the countries of collection. Calculation of the evolutionary timing of Sawadaea using molecular clocks showed that the divergence of different species of Acer occurred many millions of years before the radiation of Sawadaea. Thus, the close evolutionary relationship between Sawadaea and Acer found in this study might not be due to a true coevolutionary process. Powdery mildew fungi belonging to Sawadaea may have jumped onto Acer spp. long after the radiation of the major sections of these trees, and then expanded their host ranges according to the phylogeny and geographical distribution of Acer.