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Fusarium circinatum is an important fungal pathogen of Pinus species utilized in commercial forestry worldwide. In Colombia, it was first found on nursery plants and later in plantations associated with basal cankers on young trees. In this study, we explored the population diversity of the pathogen in Colombia by analyzing 136 isolates collected from diseased nursery plants (2005–2007) and plantation trees (2017 and 2020). These were sourced from different geographical regions and Pinus species. Genotyping was performed using 10 microsatellite markers, while mating types were identified with PCRs targeting the MAT1 locus. Using microsatellites, a total of 33 multilocus haplotypes were detected. Genetic diversity indices showed low levels of diversity in both the overall collection and in specific collection groupings. The data also suggested that a small number of isolates had unique origins in the country (p <.05), and relatively low levels of population differentiation were detected between the nursery and plantation collections. All the isolates were scored as having the MAT1‐1 mating type, and no evidence for the random association among microsatellite alleles (p =.0001) was found. Overall, these data suggest that F. circinatum was introduced into Colombia a small number of times, likely on seed for nursery production. Furthermore, the data also indicate that the pathogen has spread from nurseries to the plantations via asexual reproduction and on asymptomatic plants. This has resulted in a highly clonal F. circinatum population in Colombia that has resulted from accidental introductions of the pathogen into a production nursery. [ABSTRACT FROM AUTHOR]