Modern durum wheat (Triticum turgidum spp. durum) is a staple food crop and was domesticated from cultivated emmer wheat (T. turgidum spp. dicoccum) less than 10,000 years ago. In the process of adapting to specific growing regions, genetic diversity was lost as favorable alleles were selected by farmers and breeders. In this work, we identified over 80,000 genome-wide single nucleotide polymorphism markers in three tetraploid wheat populations including 600 cultivated emmer accessions, 161 durum landraces, and 180 breeding lines/cultivars generated by the North Dakota State University durum wheat breeding program that demark this process. We found that total genetic diversity was lost as nonfree threshing cultivated emmer populations were adapted to free-threshing durum landraces. Diversity was also lost as durum landraces were converted into modern cultivars with superior end-use quality and high yield potential in the Northern Great Plains of the U.S. Selective sweep analysis revealed specific genomic regions that underwent selection and fixation during adaption. These loci mark signals of domestication, and the underlying genes are likely involved in increasing performance of durum wheat. Markers that identify domestication/adaption alleles may be useful in screening germplasm from unadapted pools that could be readily incorporated into breeding pools to increase the diversity, or in specific gene introgression schemes to incorporate specific loci without linkage drag.