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Key message: GWAS on a bread wheat panel with high D genome diversity identified novel alleles and QTLs associated with resilience to combined heat and drought stress under natural field conditions. As heat (H) and drought stresses occur concurrently under field conditions, studying them separately offers limited opportunities for wheat improvement. Here, a wheat diversity panel containing Aegilops tauschii introgressions was evaluated under H and combined heat–drought (HD) stresses to identify quantitative trait loci (QTLs) associated with resilience to the stresses, and to assess the practicability of harnessing Ae. tauschii diversity for breeding for combined stress resilience. Using genome-wide analysis, we identified alleles and QTLs on chromosomes 3D, 5D, and 7A controlling grain yield (GY), kernel number per spike, and thousand-kernel weight, and on 3D (521–549 Mbp) controlling GY alone. A strong marker–trait association (MTA) for GY stability on chromosome 3D (508.3 Mbp) explained 20.3% of the variation. Leaf traits—canopy temperature, vegetation index, and carbon isotope composition—were controlled by five QTLs on 2D (23–96, 511–554, and 606–614 Mbp), 3D (155–171 Mbp), and 5D (407–413 Mbp); some of them were pleiotropic for GY and yield-related traits. Further analysis revealed candidate genes, including GA20ox, regulating GY stability, and CaaX prenyl protease 2, regulating canopy temperature at the flowering stage, under H and HD stresses. As genome-wide association studies under HD in field conditions are scarce, our results provide genomic landmarks for wheat breeding to improve adaptation to H and HD conditions under climate change. [ABSTRACT FROM AUTHOR]