With rising food demands, crop production on salinized lands is increasingly necessary. Sunflower, a moderately salt tolerant crop, exhibits a trade-off where more vigorous, high-performing genotypes have a greater proportional decline in biomass under salinity stress. Prior research has found deviations from this relationship across genotypes; the magnitude and direction of these deviations provides a useful metric of tolerance. Here, we identified the traits and genomic regions underlying variation in this expectation-deviation tolerance. We grew a diversity panel under control and salt-stressed conditions and measured a suite of morphological (growth, allocation, plant and leaf morphology) and leaf ionomic traits. The genetic basis of variation in these traits and their plasticity was investigated via genome-wide association studies, which also enabled the identification of genomic regions (i.e., haplotypic blocks) influencing multiple traits. We found that the magnitude of plasticity in whole root mass fraction, fine root mass fraction, and chlorophyll content, as well as leaf Na and K content under saline conditions, were the traits most strongly correlated with expectation-deviation tolerance. Additionally, we identified multiple genomic regions underlying these traits as well as a single gene directly associated with this tolerance metric. Our results show that, by taking the vigor-salinity effect trade-off into account, we can identify unique traits and genes associated with salinity tolerance. Since these traits and genomic regions are distinct from those associated with high vigor (i.e., growth in benign conditions), they provide an avenue for increasing salinity tolerance in high-performing sunflower genotypes without compromising vigor.Single sentence summaryDespite a trade-off between vigor and salinity-induced decline in biomass, distinct traits and genomic regions exist that could modulate this trade-off in cultivated sunflower.