Fusarium circinatum causes pitch canker of Pinus species in many parts of the world. The fungus was first recorded in South Africa in 1990 as a pathogen of P. patula seedlings and emerged later as a pathogen of established plantation trees, especially P. radiata in the Western Cape Province (WCP). In this study the population biology of F. circinatum in the WCP was explored. The aim was to determine the possible origin and reproductive mode of the pathogen, with the ultimate intention of informing disease management strategies in the region. Vegetative compatibility assays, sexual mating studies and amplified fragment length polymorphism analyses were used. For comparative purposes, an isolate collection obtained from diseased P. radiata seedlings in a commercial nursery in the region, as well as a set of isolates from commercial seedling nurseries in the central and northern parts of South Africa, were included. The results showed that the WCP population of F. circinatum employs a predominantly asexual mode of reproduction and that it is highly differentiated from populations of the fungus elsewhere in South Africa. However, limited genetic structure was found within the respective WCP isolate collections. Overall these findings suggest that pitch canker in the WCP originates from one or more separate introductions of the pathogen and that its movement in the region is not restricted. More effective strategies are thus required to limit and manage the effects of F. circinatum in plantations in this region of South Africa.