Genome-wide population diversity in Hymenoscyphus fraxineus points to an eastern Russian origin of European Ash dieback

European forests are experiencing extensive invasion from the Ash pathogen Hymenoscyphus fraxineus, an ecological niche competitor to the non-pathogenic native H. albidus. Here we report the genome-wide diversity and population structure in Asia (native) and Europe (the introduced range). We show H. fraxineus underwent a dramatic bottleneck upon introduction to Europe 30-70 generation ago, leaving a genomic signature characterized by long segments of fixation, interspersed with “diversity islands”. As these characteristics are identical throughout Europe no effective secondary contact with native populations has occurred. Genome-wide variation is consistently high within sampled locations in Japan and the Russian Far East, and lack of differentiation amongst Russian locations suggests extensive gene flow, similar to Europe. A local ancestry analysis supports Russian populations as a more likely source of the introduction than Japan. Negligible latency, rapid host-range expansion and viability of small founding populations specify strong biosecurity forewarnings against new introductions from outside Europe.