Cryphonectria canker caused by Cryphonectria cubensis is one of the most destructive diseases of Eucalyptus plantations in South Africa. To implement a meaningful management of plantation diseases, it is important to have an understanding of the population diversity of the pathogen. In this study, trees were surveyed to determine whether C. cubensis reproduces sexually in South Africa. The diversity of the South African C. cubensis population was assessed based on vegetative compatibility tests. Field inoculations were used to determine whether VC groups correlated with virulence. Only pycnidia were found on cankered trees, indicating that sexual reproduction does not occur. Only 23 VC groups were found amongst 100 isolates each collected from single diseased trees. A low degree of genetic diversity also indicated that sexual reproduction is absent or rare in the South African C. cubensis population. Inoculation studies revealed that isolates belonging to different VC groups differ significantly in their ability to cause lesions. The low level of genetic diversity enhances opportunities to capitalise on hypovirulence to reduce the impact of the pathogen in the future. It also supports the view that the fungus was recently introduced into South Africa.