Colletotrichum lupini, causing lupin anthracnose, is one of the worst pathogens to lupin cultivation worldwide. Understanding its population structure and evolutionary potential is crucial to design successful disease management strategies. The objective of this study was to employ population genetics to investigate the diversity, evolutionary dynamics and molecular basis of host interaction of this notorious lupin pathogen. A collection of globally representative C. lupini isolates was genotyped through triple digest restriction-site associated DNA sequencing (3D-RADseq), resulting in a dataset of unparalleled resolution. Phylogenetic and structural analysis could distinguish four (I – IV) independent lineages. The strong population structure, low recombination and slow linkage decay strongly suggests that C. lupini reproduces clonally. Different morphologies and virulence patterns on white (Lupinus albus) and Andean lupin (L. mutabilis) were observed between and within clonal lineages. Isolates belonging to lineage II were shown to have a mini-chromosome which was also partly present in lineage III and IV, but not in lineage I isolates. Variation in the presence of this mini-chromosome could indicate a role in host interaction. All four lineages were present in the South American Andes region, which is concluded to be the center of origin of this species. Only members of lineage II have been found outside South America since the 1990s, indicating it as the current pandemic population. As a seed-borne pathogen, C. lupini has mainly spread through infected but symptomless seeds, stressing the importance of phytosanitary measures to prevent future outbreaks of strains that are yet confined to South America.