<i>Zymoseptoria tritici</i> (formerly <i>Mycosphaerella graminicola</i>) is a heterothallic ascomycete causing wheat septoria tritici leaf blotch. The deployment of resistant wheat cultivars is complicated by the high diversity within populations. Sexual reproduction is frequent and contributes significantly to the high evolutionary potential of <i>Z. tritici</i>. We aimed to understand two fundamental properties of <i>Z. tritici</i>. What is the genetic basis of quantitative virulence of <i>Z. tritici</i> on wheat? How does recombination shape the evolutionary trajectory of the pathogen genome? For this, we adapted the high-throughput genotyping method based on restriction-associated DNA sequencing (RADseq). We genotyped a total of 441 progeny from two sexual crosses at over 23'000 SNP loci in order to generate a highly saturated genetic map. We successfully mapped QTLs underlying leaf necrosis and pycnidial densities for two different wheat cultivars. The genetic architecture of virulence on wheat is likely complex as QTL regions differed between the progeny populations. We found that recombination rates were highly heterogeneous along chromosomes. Recombination hotspots were preferentially located in subtelomeric regions. We found that recombination hotspots are linked to the population genomic diversity of the pathogen. The evolutionary potential of virulence genes is, hence, likely influenced by local variations in recombination rates.