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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. 

Summary Powdery mildew is an economically important disease caused byc. 1000 different fungal species.Erysiphe vacciniiis an emerging powdery mildew species that is impacting the blueberry industry. Once confined to North America,E. vacciniiis now spreading rapidly across major blueberry‐growing regions, including China, Morocco, Mexico, and the USA, threatening millions in losses.This study documents its recent global spread by analyzing both herbarium specimens, some over 150‐yr‐old, and fresh samples collected world‐wide.Our findings were integrated into a ‘living phylogeny’ via T‐BAS to simplify pathogen identification and enable rapid responses to new outbreaks. We identified 50 haplotypes, two primary introductions world‐wide, and revealed a shift from a generalist to a specialist pathogen.This research provides insights into the complexities of host specialization and highlights the need to address this emerging global threat to blueberry production.