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BACKGROUND: Prioritizing wild relative diversity for improving crop adaptation to emerging drought-prone environments is challenging. Here, we combine the genome-wide environmental scans (GWES) in wheat diploid ancestor Aegilops tauschii (Ae. tauschii) with allele testing in the genetic backgrounds of adapted cultivars to identify diversity for improving wheat adaptation to water-limiting conditions.RESULTS: We evaluate the adaptive allele effects in Ae. tauschii-wheat introgression lines phenotyped for multiple traits under irrigated and water-limiting conditions using both unmanned aerial system-based imaging and conventional approaches. The GWES show that climatic gradients alone explain more than half of genomic variation in Ae. tauschii, with many alleles associated with climatic factors in Ae. tauschii being linked with improved performance of introgression lines under water-limiting conditions. We find that the most significant GWES signals associated with temperature annual range in the wild relative are linked with reduced canopy temperature in introgression lines and increased yield.CONCLUSIONS: Our results suggest that introgression of climate-adaptive alleles from Ae. tauschii has the potential to improve wheat performance under water-limiting conditions, and that variants controlling physiological processes responsible for maintaining leaf temperature are likely among the targets of adaptive selection in a wild relative. Adaptive variation uncovered by GWES in wild relatives has the potential to improve climate resilience of crop varieties.