Technological advances in genome sequencing have rapidly improved our ability to catalog genomic variation, expanding the scope and scale of genetic studies over the past decade. Yet, for many agronomically important plant pathogens such as the downy mildews, these advances remain limited. This is, in part, due to the difficulties associated with maintaining obligate biotroph pathogens, and the logistical constraints involved in the genotyping of these species ie. obtaining DNA of sufficient quantity and quality from environmental samples. Adaptable methods such as whole genome sequencing (WGS) or reduced representation approaches for the genotyping of the downy mildews are required for the understanding of the pathogen populations from an evolutionary and ecological perspective. Here, we describe a targeted enrichment platform (TEP) able to effectively genotype isolates from two Pseudoperonospora species using DNA concentrations of less than 50 ng of mixed pathogen and plant DNA samples. We were successfully able to enrich 830 target genes across 84 samples and identified SNPs that discriminated along host preference. Future application of TEP should focus on more even distribution of targeted polymorphic regions across the pathogen genome. Our results support the ability of TEP to detect informative SNPs able to describe the population structure of Pseudoperonospora species over time and space. This platform provides an additional tool for genotyping of an obligate biotrophic plant pathogen and the execution of new genetic studies.