SignificanceFusarium oxysporumis among the most damaging of agricultural pathogens, capable of inflicting immense loss in a variety of crop species. Prevailing thought is that the organism is an exclusively asexual taxon, a notion that colors how one approaches disease control. Here, we reveal the genomic imprint of an active sexual cycle in fungal populations on chickpea. We propose that meiotic recombination generates haplotype diversity that is maintained by clonal dynamics, including restricted recombination within groups. Interestingly, these near-clonal groups derive further variation through geographically structured variation in a large accessory genome. These observations have implications for disease management and forecasting of pathogenic forms, not only in chickpea, but in all crop species impacted by the globally distributedF. oxysporumpathogen.