Soil salinization poses a threat to maize production worldwide, but the genetic mechanism of salt tolerance in maize is not well understood.  Therefore, identifying the genetic components underlying salt tolerance in maize is of great importance.  In the current study, a teosinte-maize BC₂F₇ population was used to investigate the genetic basis of 21 salt tolerance-related traits.  In total, 125 QTLs were detected using a high-density genetic bin map, with one to five QTLs explaining 6.05–32.02% of the phenotypic variation for each trait.  The total phenotypic variation explained (PVE) by all detected QTLs ranged from 6.84 to 63.88% for each trait.  Of all 125 QTLs, only three were major QTLs distributed in two genomic regions on chromosome 6, which were involved in three salt tolerance-related traits.  In addition, 10 pairs of epistatic QTLs with additive effects were detected for eight traits, explaining 0.9 to 4.44% of the phenotypic variation.  Furthermore, 18 QTL hotspots affecting 3–7 traits were identified.  In one hotspot (L5), a gene cluster consisting of four genes (ZmNSA1, SAG6, ZmCLCg, and ZmHKT1;2) was found, suggesting the involvement of multiple pleiotropic genes.  Finally, two important candidate genes, Zm00001d002090 and Zm00001d002391, were found to be associated with salt tolerance-related traits by a combination of linkage and marker-trait association analyses.  Zm00001d002090 encodes a calcium-dependent lipid-binding (CaLB domain) family protein, which may function as a Ca²⁺ sensor for transmitting the salt stress signal downstream, while Zm00001d002391 encodes a ubiquitin-specific protease belonging to the C19-related subfamily.  Our findings provide valuable insights into the genetic basis of salt tolerance-related traits in maize and a theoretical foundation for breeders to develop enhanced salt-tolerant maize varieties.