The genus Cucurbita (pumpkin), encompassing C. maxima and C. moschata, is agriculturally and nutritionally significant globally. Herein, we re-sequenced 146 germplasm accessions (51 C. moschata and 95 C. maxima) to characterize genomic variations and identify loci associated with critical traits. Population structure analysis revealed four distinct subgroups: G1 (C. moschata), and G2–G4 (C. maxima), the latter classified by rind color (green, gray, and red, respectively). A genome-wide association study (GWAS) analysis identified 26 loci associated with eight fruit quality traits (e.g., rind color, pulp thickness, starch content) and leaf traits. Selective sweep analyses revealed 18 overlapping signals between the GWAS and selective regions, highlighting convergent evolution in starch content, pulp thickness, and water content driven by artificial and natural selection. We further validated these key fruit quality candidate genes, confirming that starch, cellulose, and pulp trait-related genes exhibited genotype-specific expression consistent with the quality divergence between CMO-X and CMO-E. Notably, C. moschata exhibited higher β-carotene and water content, while C. maxima showed higher starch content, reflecting divergent selection pressures. For leaf traits, 13 loci associated with leaf length were found, including LL9.2/LW9.1 with Cmax09G001045, which regulates leaf size. A novel haplotype in Cmax09G001045 explained the small-leaf phenotype of ‘Cuili 5’. This study provides a comprehensive genomic variation map of C. maxima and C. moschata, clarifies the genetic bases of key agronomic traits, and sheds light on their domestication and selection history, offering valuable resources for molecular breeding and crop improvement.
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