Cucurbit downy mildew (DM), caused by the obligate biotrophic oomycete Pseudoperonospora cubensis, is a major foliar disease of cucumber. Cucumber accession PI197088 was previously shown to be one of the most promising donors for DM resistance. The resistance in PI197088 is controlled by multiple quantitative trait loci (QTL), each with a relatively small effect. We developed a cucumber line with a 12 Mb introgression from PI197088 in a susceptible background. This introgression line was partially resistant to DM. Subsequently, we combined fine mapping data with RNAseq and whole genome resequencing to identify candidate genes for the resistance conferred by this introgression. Interestingly, fine-mapping data suggested that the partial resistance is caused by a combination of multiple genetically linked genes, leading to three subQTL, each with a different effect on the disease phenotype. In one of these subQTL we identified several Receptor Like Kinase genes (RLK). A novel RLK gene appeared to be present in resistant genotypes. In susceptible genotypes, including the reference genotype “Chinese Long 9930”, this novel gene has a 551 base pair deletion, and was therefore not correctly predicted during the annotation of the cucumber genome. In another subQTL, we found a loss-of-function mutation in the novel susceptibility gene (S-gene) CsAAP2A, encoding an amino acid transporter. In the resistant genotype a non-functional allele of this gene is present due to integration of a transposable element in its coding sequence.