The native European ash fungus Hymenoscyphus albidus is threatened by the morphologically similar introduced ash dieback pathogen Hymenoscyphus fraxineus. H. fraxineus is heterothallic and its populations comprise numerous different vegetative compatibility (vc) types. H. albidus is homothallic with unknown population diversity. In vitro pairings of H. albidus isolates from one French and three UK sites showed compatible (intermingling) and incompatible (gap) reactions similar to those in H. fraxineus. Local vc diversity was high with vc types per isolate ranging from ca. 0.7 to 0.9 and the probability of any two isolates being incompatible ca. 93–98%; suggesting at least four biallelic vic loci in each population. Pairings between single ascospore isolates from the same apothecium, however, were uniformly compatible. All rachis and single ascospore isolates had both MAT1-1-3 and MAT1-2-1 mating type genes, consistent with homothallism. The results suggest local H. albidus populations comprise numerous, vegetatively incompatible genets maintained in part by haploid selfing.