Cucumber crops face high pressure from pathogens, including various viral species. Mapping quantitative trait loci (QTL) for vegetable resistance to viruses has primarily been conducted after mechanical inoculation in controlled environments, but not in crop field conditions. Moreover, viruses that cannot be mechanically inoculated, e.g. the cucurbit aphid-borne yellows virus (CABYV), have been overlooked in resistance studies. Here, we aimed to identify QTLs reducing epidemics of two prevalent cucumber viruses: CABYV and the cucumber mosaic virus (CMV). We evaluated the resistance of 256 elite cucumber lines and landraces in crop field conditions by screening for the presence of both viruses six-times during the season. We mapped twelve QTLs reducing CABYV epidemics and seven QTLs reducing CMV epidemics by combining multiloci genome-wide association studies and local score approach analyses. We also examined the attractiveness of this cucumber panel for Aphis gossypii, a major cucumber virus vector. We identified five QTLs that reduced the attractiveness, including one co-localizing with a QTL reducing CABYV epidemics. Interestingly, some accessions deemed CMV-resistant after mechanical inoculation in controlled environments showed high infection rates in crop field conditions. Only one QTL for CMV resistance was detected in both conditions, indicating that these phenotypes are regulated by independent QTLs. Local linkage disequilibrium study findings suggested that certain QTLs reducing epidemics were introduced early into elite lines through serendipity or selection. QTLs could be pyramided with other low-effect QTLs through genomic selection to obtain cucumber cultivars with enhanced field resistance to viruses.