Soil salinity severely limits grapevine yield and fruit quality; however, the mechanisms underlying salt tolerance remain poorly understood. Small secreted peptides, particularly rapid alkalinization factor (RALF) peptides, are key regulators of plant responses to environmental stress. However, a systematic analysis of the RALF gene family in grapevine (Vitis vinifera L.) has not been conducted. In this study, we identified 11 VvRALFs in the grapevine genome (PN_T2T) and characterized their physicochemical properties, structural features, and evolutionary relationships. Expression profiling revealed that VvRALF9 was consistently upregulated in the roots of the salt-sensitive rootstock ‘Beta’ but downregulated in the salt-tolerant rootstock ‘3309C’. Silencing VvRALF9 in the roots of grapevine rootstocks significantly enhanced their salt tolerance. Protein interaction assays, including yeast two-hybrid, split-LUC, and pull-down assays, identified VvFER2 as a potential receptor of VvRALF9. Overexpression of VvFER2 in the roots of grapevine rootstocks also improved salt tolerance. Transcriptomic analysis of VvRALF9-RNAi roots revealed significant enrichment of the plant hormone signal transduction pathway, together with extensive changes in the expression of transcription factors and genes associated with multiple hormone signaling pathways. Together, these findings suggest that the VvRALF9–VvFER2 module is involved in the regulation of grapevine salt stress responses.