Understanding of the genetic mechanism of heat tolerance (HT) can accelerate and improve wheat breeding in dealing with a warming climate. This study identified and validated quantitative trait loci (QTL) responsible for HT in common wheat. The International Triticeae Mapping Initiative (ITMI) population, recombinant inbreed lines (RILs) derived from a cross between Synthetic W7984 and Opata M85, was phenotyped for shoot length, root length, whole plant length under heat stress and corresponding damage indices (DIs) to compare HT performances of individuals. Wide variations among the RILs were shown for all the traits. A total of 13 QTL including 9 major QTL and 4 minor QTL were identified, distributed on 6 wheat chromosomes. The six major QTL with the highest R2 were associated with different traits under heat stress. They were all from Opata M85 background and located within a 2.2 cm interval on chromosome 4D, making up a QTL hotspot conferring HT in common wheat. The QTL hotspot was validated by genotyping-phenotyping association analysis using single-nucleotide-polymorphism (SNP) assays. The QTL, especially the 4D QTL hotspot identified and validated in this study, are valuable for the further fine mapping and identification of key genes and exploring genetic mechanism of HT in wheat.