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Watermelon (Citrullus spp.) is an economically important crop globally, but it is susceptible to various diseases, including powdery mildew. Previous studies have identified genetic factors associated with powdery mildew resistance. However, further research using diverse genetic approaches is necessary to elucidate the underlying genetic mechanisms of this resistance. In this study, the germplasm collection comprising highly homozygous inbred lines was employed, which enabled the accumulation of consistent data and improved the reliability of the genome-wide association study (GWAS) findings. Our investigation identified two significant single-nucleotide polymorphisms (SNPs), pm2.1 and pm3.1, which were strongly associated with disease resistance. Moreover, several candidate genes were revealed within the linkage disequilibrium (LD) blocks surrounding the significant SNPs. In conclusion, the identification of significant SNPs and their additive effects, combined with the discovery of relevant candidate genes, expanded our understanding of the genetic basis of disease resistance and can pave the way for the development of more resilient watermelon cultivars through marker-assisted selection.