Salinity is a major abiotic stress in wheat production across the globe, especially in arid and semi-arid areas. In this study, 313 genetically diverse wheat genotypes were assessed for vegetative-stage salinity tolerance in a hydroponic condition and genotyped using 35K Axiom SNP array. Genotyping of the 313 wheat genotypes produced 24,968 polymorphic SNPs. To dissect salt tolerance, marker-trait association analysis was carried out using the salt tolerance indices of three traits, such as leaf chlorophyll content, green leaf area, and dry biomass. In total, 24 quantitative trait nucleotides (QTNs) showing significant associations with these three traits were identified, including seven linked to leaf chlorophyll content, twelve with green leaf area, and five to dry biomass traits. Four QTNs (Q.CCI-E3-1A, Q.CCI-E3-5D, Q.DB-E3-1B, and Q.GLA-E3-5A.2) showed significant phenotypic effects and represented GWAS-significant loci under both control and salt-stress conditions. Gene ontology analysis of the genomic regions linked to these QTNs revealed 67 putative candidate genes associated with ion transport, stress signaling, and photosynthetic processes. The identified SNPs, QTNs, and candidate genes provide valuable genomic resources for marker-assisted breeding of salt-tolerant wheat cultivars, contributing to sustainable wheat production under saline environments.