In arid and semi-arid regions, huge agricultural lands are affected by salinity, and the influence of salt is aggravated by high temperature. The previous studies considered heat and salinity as isolated stress elements, and to the best of our knowledge, no reports elucidated the wheat response to the combined heat-salinity stress. We phenotyped 247 multiple synthetic derivatives lines for ten yield and yield-related traits under combined heat and salinity stress in the field for two seasons. The genotypes, seasons and their interaction were significant for most of the traits. The heritability of the traits varied from low in chlorophyll content (≤0.5) to high (≥0.7) in grain yield in the first season and days to heading in the second season. Tiller number, grain per spike, biomass and harvest index were the most contributing traits to grain yield under the combined stress and could be good selection criteria. We identified 46 tolerant lines, of which five were stable and could be used as parents in breeding as well as in further studies to uncover the physiological and genetic mechanisms of the combined heat-salinity stress tolerance. Most of the tolerant lines identified were derivatives of the Ae. tauschii accession KU-2156 collected from saline soil in Iran. GWAS was performed using 14356 SNP and silico-DArT markers. The results revealed 146 significant marker-trait associations, out of which, 23 were stable across the seasons. Interestingly, 65.7% of these significant associations were from the D genome. We identified two heat stress transcription factors putative genes Traes_2AS_CF07F4EC2 and Traes_2DS_B6872CB84 on chromosomes 2AS and 2DS, respectively. Incorporation of the favorable alleles identified after validation would improve wheat yield under the combined stress condition. The study demonstrated the value of wheat progenitor Ae. tauschii as a rich genetic resource to improve wheat heat and salinity stress tolerance and further proved the suitability of the multiple synthetic derivatives population as an effective platform for gene mining in Ae. tauschii.