Powdery mildew infections are among the most severe foliar biotrophic fungal diseases in grain legumes. Several accessions of Lathyrus cicera (chickling pea) show levels of partial resistance to Erysiphe pisi, the causal agent of pea powdery mildew, and to E. trifolii, a powdery mildew pathogen recently confirmed to infect pea and Lathyrus spp. Nevertheless, the underlying L. cicera resistance mechanisms against powdery mildews are poorly understood. To unveil the genetic control of resistance against powdery mildews in L. cicera, a recombinant inbred line population segregating for response to both species was used in resistance linkage analysis. An improved L. cicera genetic linkage map was used in this analysis. The new higher-density linkage map contains 1,468 polymorphic loci mapped on seven major and two minor linkage groups, covering a total of 712.4 cM. The percentage of the leaf area affected by either E. pisi or E. trifolii was recorded in independent screenings of the recombinant inbred line population, identifying a continuous range of resistance-susceptibility responses. Distinct quantitative trait loci (QTLs) for partial resistance against each pathogen were identified, suggesting different genetic bases are involved in the response to E. pisi and E. trifolii in L. cicera. Moreover, through comparative mapping of L. cicera QTL regions with the pea reference genome, candidate genes and pathways involved in resistance against powdery mildews were identified. This study extended the previously available genetic and genomic tools in Lathyrus species, providing clues about diverse powdery mildew resistance mechanisms useful for future resistance breeding of L. cicera and related species.