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Plants with shorter internodes are suitable for high-density planting, lodging resistance and the preservation of land resources by improving yield per unit area. In this study, we identified a locus controlling the short internode trait in watermelon using Zhengzhouzigua (long internode) and Duan125 (short internode) as mapping parents. Genetic analysis indicated that F₁ plants were consistent with long internode plants, which indicates that the long internode was dominant over the short internode. The observed F₂ and BC₁ individuals fitted the expected phenotypic segregation ratios of 3:1 and 1:1, respectively. The locus was mapped on chromosome 9 using a bulked segregant analysis approach. The region was narrowed down to 8.525 kb having only one putative gene, <i>Cla015407</i>, flanking by CAPS90 and CAPS91 markers, which encodes gibberellin 3&#946;-hydroxylase (GA 3&#946;-hydroxylase). The sequence alignment of the candidate gene between both parents revealed a 13 bp deletion in the short internode parent, which resulted in a truncated protein. Before GA₃ application, significantly lower GA₃ content and shorter cell length were obtained in the short internode plants. However, the highest GA₃ content and significant increase in cell length were observed in the short internode plants after exogenous GA₃ application. In the short internode plants, the expression level of the <i>Cla015407</i> was threefold lower than the long internode plants in the stem tissue. In general, our results suggested that <i>Cla015407</i> might be the candidate gene responsible for the short internode phenotype in watermelon and the phenotype is responsive to exogenous GA₃ application.