Plasmopara viticola, the causal agent of grapevine downy mildew, is a biotrophic oomycete engaged in a tight coevolutionary relationship with its host. Rapid adaptation of the pathogen is favored by annual sexual reproduction that generates genotypic diversity. With the aim of studying the recombination landscape across the P. viticola genome, we generated 2 half-sibling F1 progenies (N = 189 and 162). Using targeted SNP sequencing, between 1,405 and 1,894 markers were included in parental linkage maps, and a consensus map was obtained by integrating 4,509 markers. The reference genome could be assembled into 17 pseudochromosomes, anchoring 88% of its physical length. We observed a strong collinearity between parental genomes and extensive synteny with the downy mildew Peronospora effusa. In the consensus map, the median recombination rate was 13.8 cM/Mb. The local recombination rate was highly variable along chromosomes, and recombination was suppressed in putative centromeric regions. Recombination rate was found negatively correlated with repeats’ coverage and positively correlated with gene coverage. However, genes encoding secreted proteins and putative effectors were underrepresented in highly recombining regions. In both progenies, about 5% of the individuals presented karyotypic anomalies. Aneuploidies and triploidies almost exclusively originated from the male-transmitted chromosomes. Triploids resulted from fertilization by diploid gametes, but also from dispermy. Obligatory sexual reproduction each year may explain the lower level of karyotypic variation in P. viticola compared to other oomycetes. The linkage maps will be useful to guide future de novo chromosome-scale assemblies of P. viticola genomes and to perform forward genetics.