Cryphonectria parasitica is an invasive fungal pathogen that causes blight disease on chestnut trees. Its destructive effect can be controlled with naturally occurring mycovirus Cryphonectria hypovirus 1 (CHV1). To date, the spread of C. parasitica and CHV1 in Europe is fairly well documented, but there are still several unexplored regions. Thus, we sampled blight cankers from four sweet chestnut populations in Bay of Kotor and Lake Skadar regions in Montenegro. We determined vegetative compatibility (vc) type and mating-type diversity using molecular vic and MAT1 genotyping, as well as confirming the presence of CHV1 by RT-PCR. We identified 11 vc types, with EU-12 being the dominant one represented by 58.2% of all fungal isolates. The Shannon diversity index ranged from 0.93 to 1.47. Both mating types of C. parasitica were found in all four populations. The prevalence of CHV1 ranged from 15% to 40%. All CHV1 isolates belonged to Italian subtype I of CHV1 and were closely related, with relatively recent common ancestors. Our results indicate a longer presence of C. parasitica and CHV1 in Montenegro than previously thought. Natural biocontrol with CHV1 seems to be well established. However, it has the potential for deterioration; thus, close monitoring is required.