Wild emmer wheat (WEW), the progenitor of most cultivated wheat species, evolved in the Fertile Crescent about 0.5 million years ago. The large size of the wheat genome, its polyploidy, and its high content of repetitive elements delayed the construction of a comprehensive reference genome for many years. However, despite the difficulties, a high-quality polyploid genome assembly of the wild emmer wheat accession “Zavitan” was published in 2017, presenting 14 chromosome-scale assemblies (pseudomolecules) with a total size of 10.1 Gb, as well as one group of unanchored scaffolds (0.4 Gb). Integration of an optical map enabled improvement of assembly parameters and the annotation of 97,908 genes. In this chapter, we aligned exome-capture data of 134 WEW accessions from the Fertile Crescent to the Zavitan genome assembly and describe the population structure. Admixture and PCA (principal component analysis) analyses revealed three genetically separate groups. We defined these three groups according to their geographical and morphological characteristics as narrow-spike WEW from Turkey, Iraq, and Iran (northeastern [NE]-Horanum group); narrow-spike WEW from the southwestern (SW) Fertile Crescent (SW-Horanum group); and wide-spike WEW from SW Fertile Crescent (SW-Judaicum group). We found that the SW-Horanum group exhibited the highest diversity, thus representing the core of WEW’s diversity. Moreover, we demonstrated the genetic uniqueness of the SW-Judaicum group by focusing on a region close to the flowering induction VRN1-A gene. Finally, we review the use of WEW’s genomic resources and genome reference in recent years. The WEW gene pool has been used in wheat breeding programs to improve disease resistance and other desirable agricultural traits. It has also been used to study wheat’s genetic evolution and domestication processes. These advances improve our food security as well as increase basic and applied knowledge. Considering that only the Zavitan genome, belonging to the unique SW-Judaicum group, was sequenced, we propose that more reference genomes, preferably from the other groups, should be assembled and become publicly available.