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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.