Tree diseases constitute a significant threat to biodiversity worldwide. Pathogen discovery in natural habitats is of vital importance to understanding current and future threats and prioritising efforts towards developing disease management strategies. Ash dieback is a fungal disease of major conservational concern that is infecting common ash trees,Fraxinus excelsior, in Europe. The disease is caused by a non-native fungal pathogen,Hymenoscyphus fraxineus. Other dieback causing-species have not previously been identified in the genusHymenoscyphus. Here, we discover the pathogenicity potential of two newly identified related species of Asian origin,H. koreanusandH. occultus, and one Europe-native related species,H. albidus. We sequence the genomes of all threeHymenoscyphusspecies and compare them to that ofH. fraxineus. Phylogenetic analysis of core eukaryotic genes identifiedH. albidusandH. koreanusas sister species, whilstH. occultusdiverged prior to these andH. fraxineus. All fourHymenoscyphusgenomes are of comparable size (55–62 Mbp) and GC contents (42–44%) and encode for polymorphic secretomes. Surprisingly, 1133 predicted secreted proteins are shared between the ash dieback pathogenH. fraxineusand the three relatedHymenoscyphusendophytes. Amongst shared secreted proteins are cell death-inducing effector candidates, such as necrosis, and ethylene-inducing peptide 1-like proteins, Nep1-like proteins, that are upregulated duringin plantagrowth of allHymenoscyphusspecies. Indeed, pathogenicity tests showed that all four relatedHymenoscyphusspecies develop pathogenic growth on European ash stems, with nativeH. albidusbeing the least virulent. Our results identify the threatHymenoscypohusspecies pose to the survival of European ash trees, and highlight the importance of promoting pathogen surveillance in environmental landscapes. Identifying new pathogens and including them in the screening for durable immunity of common ash trees is key to the long-term survival of ash in Europe.Supplementary InformationThe online version contains supplementary material available at 10.1186/s43008-023-00115-8.