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Acer(Sapindaceae) is a major genus of broadleaf trees dominating deciduous forests in the Northern Hemisphere, with Asia exhibiting the highest species diversity. Many economically importantAcerspecies are cultivated for ornamental or timber purposes.Acerpowdery mildew, caused by fungi in the tribeCystotheceae, poses significant global economic and ecological threats. The pathogenicity spectrum remains unclear due to taxonomic uncertainties in its primary causal genera,SawadaeaandTakamatsuella. This study presents a comprehensive phylogenetic-taxonomic analysis of the two genera across East Asia, Europe, and North America. Using 75 ITS and 58 28S rDNA newly obtained sequences, we resolved 12Sawadaeaspecies and oneTakamatsuellaspecies into nine monophyletic clades, revealing marked cryptic diversity (three new species:S. acerina,S. aceris-arguti,S. taii) and two paraphyletic groups (S. bifida/S. negundinis). Taxonomic revisions include:S. bicornissplit into twoformae(f. bicornisandf. polyphaga f. nov.) with distinct host preferences;S. tulasnei(sensu stricto) restricted to Europe/North America, invalidating previous Asian records;S. nankinensisandS. koelreuteriaeform two basal lineages. Phylogenetic positioning confirmedTakamatsuellaas a distinct genus sister toSawadaea, supported by an ITS1 26 bp deletion. Host specificity analysis revealed narrow host ranges (primarilyAcer) with two evolutionary host expansions toKoelreuteria,Aesculus, andLiquidambar. This study also newly describes the asexual morphs of four species (S. aesculi,S. bifida,S. bomiensisandS. kovaliana) and establishes a molecular framework for disease management through clarified phylogeny and taxonomy. Our findings provide critical insights into fungal evolution, host-pathogen interactions, and strategies for mitigating powdery mildew impacts in forest ecosystems.