Understanding the genetic diversity and structure of invasive pathogens in source and introduced areas is crucial to reveal hidden biological aspects of an organism, to reconstruct the course of invasions and to establish effective control measures. Hymenoscyphus pseudoalbidus (anamorph: Chalara fraxinea) is an invasive and highly destructive fungal pathogen on common ash Fraxinus excelsior in Europe and occurs natively in east Asia. To get insights into the dispersal mechanism and the history of invasion, we used microsatellite markers and characterized the genetic structure and diversity of H. pseudoalbidus populations at three spatial levels: (i) in Europe; (ii) at the epidemic front and (iii) between Europe and Japan. The 1208 European strains form one large population as no evident structure was detected using Bayesian and multivariate clustering analysis. Only the distribution of genetic diversity in space, pairwise population differentiation (GST) and the spatial analysis of principal components revealed a faint geographic pattern around Europe. A significant allele deficiency in most European populations pointed to a recent genetic bottleneck whereas no pattern of isolation by distance was found. Populations from Japan harbored a higher genetic diversity and were genetically differentiated from European ones. Nevertheless, phylogenetic and network analysis clearly demonstrated that individuals from both regions are conspecific. Our data suggest that H. pseudoalbidus was introduced only once by a minimum of two individuals. The potential source region of H. pseudoalbidus is huge and further investigations are required for a more accurate localization of the source population.