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With the increase in watermelon cultivation area, there is an urgent need to explore enzymatic and genetic resources for the sustainable development of watermelon, especially under salt stress. Among the various compounds known, trehalose plays an important role in regulating abiotic stress tolerances in diverse organisms, including plants. Therefore, the present study comprehensively analyzed the trehalose-6-phosphate synthase (<i>TPS</i>) gene family in watermelon. The study analyzed the functional classification, evolutionary characteristics, and expression patterns of the watermelon <i>TPS</i> genes family. Seven <i>ClTPSs</i> were identified and classified into two distinct classes according to gene structure and phylogeny. Evolutionary analysis suggested the role of purifying selection in the evolution of the <i>TPS</i> family members. Further, <i>cis-</i>acting elements related to plant hormones and abiotic stress were identified in the promoter region of the <i>TPS</i> genes. The tissue-specific expression analysis showed that <i>ClTPS</i> genes were widely expressed in roots, stems, leaves, flowers, and fruits, while <i>ClTPS3</i> was significantly induced under salt stress. The overexpression of <i>ClTPS3</i> in <i>Arabidopsis thaliana</i> significantly improved salt tolerance. Finally, the STRING functional protein association networks suggested that the transcription factor ClMYB and ClbHLH regulate <i>ClTPS3</i>. Thus, the study indicates the critical role of <i>ClTPS3</i> in watermelon response to salt stress.