Drought and heat are major concerns for wheat production as they dramatically reduce grain yield. Climate change is predicted to lead to more episodes of drought and heat and requires the breeding of tolerant cultivars able to sustain production under stress. A multi-environment analysis of a double-haploid population of a cross between two wheat cultivars RAC875 (high yielding under drought) and Kukri (low yielding under drought) enabled the detection of a quantitative trait locus (QTL) qDHY.3BL on chromosome 3BL. The RAC875 allele was associated with an increase in grain and plant biomass under drought and heat stress. The development of 47 gene-based molecular markers for fine mapping, coupled with whole genome sequencing data of the parental lines, and the analysis of recombinant inbred lines using the multi-environment model allowed us to narrow down the QTL interval. Compared with the reference Chinese Spring x Renan genetic map, a chromosomal rearrangement in RAC875 x Kukri reduced the interval further from 3.5 Mbp in Chinese Spring to ~710 Kbp. We defined a list of 22 genes within this interval. Finally, we identified haplotypes at the QTL interval from a diverse wheat panel combining 800 worldwide accessions and studied their distribution among these accessions. The positive RAC875 allele was rare and represents a valuable source of abiotic stress tolerance.