Colletotrichum tanaceti is an emerging fungal pathogen in commercially grown Pyrethrum (Tanacetum cinerarifolium) fields in Australia. Whole genome assembly of C. tanaceti was used to develop a polymorphic microsatellite marker library of 11 loci which was then used to determine the diversity and structure of pathogen populations. Genotyping 191 isolates from hierarchical sampling conducted in 2013, from three sites in Tasmania and in 2016, from two in Tasmania and one in Victoria revealed an increase in overall haploid diversity over time. The least pairwise population distance was between two sites in the same locality;Table Cape, suggesting some level of genetic structure. However, the second least distance was between two sites from 2016 in Victoria and Tasmania. Low number of private alleles between these two sites suggested the populations maybe sharing a source of inoculum causing them to have a similar genetic composition despite their geographical distribution. Analysis of molecular variance showed the presence of significant differentiation only within samples but showed no evidence of structure over year, localities or fields, supporting the null hypothesis of a single panamictic population. Linkage disequilibrium analysis revealed that recombination was a widespread phenomenon in all populations from Tasmania where populations were not significantly different from randomised hypothetical datasets, providing evidence of sexual reproduction. Even though the Victorian population appeared asexual, after clone correcting that too confirmed to be in linkage equilibrium, suggesting low level of sexual reproduction.However, the presence of only 176 original multilocus genotypes from 191 haploid individuals indicated partial clonality, hence a mixed reproduction system. Pathogen populations with less geographic differentiation and mixed reproduction strategy have higher evolutionary risk. In C. tanaceti, this is elevated by producing both splash dispersed and airborne spores and a heterothallic mating strategy. Therefore these findings emphasise the necessity for conducting strict management practices at planting.