Powdery mildew (PM) is one of the most serious diseases in cucumber and causes huge yield loss. Multiple quantitative trait loci (QTLs) for PM resistance have been reported in previous studies using a limited number of cucumber accessions. In this study, a cucumber core germplasm (CG) consisting of 94 resequenced lines was evaluated for PM resistance in four trials across three years (2013, 2014, and 2016). These trials were performed on adult plants in the field with natural infection. Using genome-wide association study (GWAS), 13 loci (pmG1.1, pmG1.2, pmG2.1, pmG2.2, pmG3.1, pmG4.1, pmG4.2, pmG5.1, pmG5.2, pmG5.3, pmG5.4, pmG6.1, and pmG6.2) associated with PM resistance were detected on all chromosomes except for Chr.7. Among these loci, ten were mapped to chromosomal intervals where QTLs had been reported in previous studies, while, three (pmG2.1, pmG3.1, and pmG4.1) were novel. The loci of pmG2.1, pmG5.2, pmG5.3 showed stronger signal in four trials. Based on the annotation of homologous genes in Arabidopsis and pairwise LD correlation analysis, candidate genes located in the QTL intervals were predicted. SNPs in these candidate genes were analyzed between haplotypes of highly resistant (HR) and susceptible (HS) CG lines, which were defined based on combing disease index data of all trials. Furthermore, candidate genes (Csa5G622830 and CsGy5G015660) reported in previous studies for PM resistance and cucumber orthologues of several PM susceptibility (S) genes (PMR5, PMR-6, and MLO) that are colocalized with certain QTLs, were analyzed for their potential contribution to the QTL effect on both PM and DM in the CG population. This study shows that the CG germplasm is a very valuable resource carrying known and novel QTLs for both PM and DM resistance, which can be exploited in cucumber breeding.