The Fusarium oxysporum species complex (FOSC) is a group of closely related plant pathogens long-considered strictly clonal, as sexual stages have never been recorded. Several studies have questioned whether recombination occurs in FOSC, and if it occurs its nature and frequency are unknown. We analysed 410 assembled genomes to answer whether FOSC diversified by occasional sexual reproduction interspersed with numerous cycles of asexual reproduction akin to a model of predominant clonal evolution (PCE). We tested the hypothesis that sexual reproduction occurred in the evolutionary history of FOSC by examining the distribution of idiomorphs at the mating locus, phylogenetic conflict and independent measures of recombination from genome-wide SNPs and genes. A phylogenomic dataset of 40 single copy orthologs was used to define structure a priori within FOSC based on genealogical concordance. Recombination within FOSC was tested using the pairwise homoplasy index and divergence ages were estimated by molecular dating. We called SNPs from assembled genomes using a k-mer approach and tested for significant linkage disequilibrium as an indication of PCE. We clone-corrected and tested whether SNPs were randomly associated as an indication of recombination. Our analyses provide evidence for sexual or parasexual reproduction within, but not between, clades of FOSC that diversified from a most recent common ancestor about 500 000 years ago. There was no evidence of substructure based on geography or host that might indicate how clades diversified. Competing evolutionary hypotheses for FOSC are discussed in the context of our results.