Elymus sensu stricto includes tetraploid species in the tribe Triticeae with a StH genome combination derived from Hordeum (H) and Pseudoroegneria (St). The group is related to many important cereals and forage grasses and is considered an important wild genetic resource for crop breeding. The relationships within Elymus s.s. have been difficult to resolve due to the large number of widely distributed species, a high degree of morphological diversity, introgression between species, and potential multiple origins. Using genome-wide DArTseqLD data from 57 taxa, including the StH group and associated species, it is possible to gain representative information about the genetic structure of the genus. SplitsTree, STRUCTURE and principal component analysis (PCoA) show that Elymus s.s. is divided into two major clades highly correlating with geographical origin separating American species from Eurasians. These findings, together with the contribution of different Pseudoroegneria and Hordeum species to the two clades, support the conclusion that Elymus s.s. has at least two independent origins. The Eurasian and American clades are further divided into three and two subclades, respectively. The results show that Elymus species have migrated multiple times from North to South America and between America and Eurasia. The new findings could be used to develop a new classification of Elymus s.s. with sections based on phylogenetic data.