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Salt stress is a major constraint to crop productivity and quality. The limited availability of salt-tolerant genes poses significant challenges to breeding programs aimed at enhancing salt tolerance. Sorghum displays a remarkable ability to withstand saline conditions; therefore, elucidating the genetic underpinnings of this trait is crucial. This study entailed a comprehensive resequencing of 186 sorghum accessions to perform a genome-wide association study (GWAS) focusing on relative root length (RL) and root fresh weight (RFW) under salt stress conditions. We identified eight candidate genes within a co-localized region, among which SbTEF1—a gene encoding a transcription elongation factor protein—was deemed a potential candidate due to its annotation and expression pattern alterations under salt stress. Haplotype analysis, gene cloning, linkage disequilibrium (LD) analysis, and allele effect analysis revealed that PAV284, located in the promoter region of SbTEF1, modulated gene expression under salt stress, which, in turn, influenced sorghum seedlings’ salt tolerance. PAV284 holds promise as a genetic marker for the selection of salt-tolerant germplasm via marker-assisted breeding, enhancing the development of salt-tolerant sorghum cultivars.