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Powdery mildew (PM) is one of the most destructive fungal diseases, reducing the productivity of Cucurbita crops globally. In the present study, the zucchini inbred line ‘X10’ had highly stable PM resistance at the key time of inoculation (6 hpi to 48 hpi), and ‘Jin234’ showed PM susceptible. Genetic analysis revealed that PM resistance in ‘X10’ is controlled by one major dominant locus, CpPM10.1 . Based on the strategy of QTL-seq combined with linkage analysis and the Kompetitive Allele-Specific PCR (KASP) method, CpPM10.1 was located in a 382.9 kb region on chromosome 10. Using 1,400 F 2 individuals and F 2:3 offspring of the recombinants, CpPM10.1 was defined as a region of approximately 20.9 kb that contained 5 coding genes. Among them, Cp4.1LG10g02780 , Cp4.1LG10g02800 and Cp4.1LG10g02750 contained a RPW8 domain, which controls resistance to a broad range of PM pathogens. Nonsynonymous SNPs existed between ‘X10’ and ‘Jin234’ in Cp4.1LG10g02780 and Cp4.1LG10g02750 . Furthermore, the expression of Cp4.1LG10g02780 in ‘X10’ and the R-F2 pool was significantly higher than that in ‘Jin234’ and the S-F2 pool at the key period of inoculation, which showed that the expression of Cp4.1LG10g02780 was strongly positively involved in PM resistance. Further allelic diversity analysis in zucchini germplasm resources indicated that PM resistance associated with two SNPs in the RPW8 domain of Cp4.1LG10g02780 . This study not only provides highly stable PM resistance gene resources in cucurbit crops but also lays the foundation for the functional analysis of PM resistance and resistance breeding in zucchini.