Chestnut blight has spread throughout Europe since the introduction of its causal agent Cryphonectria parasitica over 70 years ago. In our study, we have analysed diversity of vegetative compatibility (vc) and microsatellite genotypes of C. parasitica, as well as sequence diversity of Cryphonectria hypovirus 1 (CHV1) in six populations from Switzerland, Croatia and North Macedonia. Resampling of local populations that were already investigated more than a decade ago allowed us to analyse the spatial and temporal population structure across an invasive range of the pathogen in Europe. Regardless which genetic marker was used, the over 60 year-old Swiss and Croatian populations had a high population diversity, while more recent North Macedonian populations were mostly clonal. These diversity differences between the investigated populations remained stable over time. A high diversity of CHV1 was observed in all three countries, with North Macedonian strains forming a separate cluster from strains obtained in other countries. No correlation between vc diversity and CHV1 prevalence was observed, suggesting a well-established and maintained natural hypovirulence in all countries, further corroborated by an observed increase in genetic diversity of Croatian C. parasitica populations over time, without collapse of CHV1 prevalence.