Phylogenetic origin of the Y haplome present in allopolyploid Triticeae species remains unknown. Here, we report the 10.47 Gb chromosome-scale genome of allohexaploid Elymus nutans (StStYYHH). Phylogenomic analyses reveal that the Y haplome is sister to the clade comprising V and Jv haplomes from Dasypyrum and Thinopyum. In addition, H haplome from the Hordeum-like ancestor, St haplome from the Pseudoroegneria-like ancestor and Y haplome are placed in the successively diverged clades. Resequencing data reveal the allopolyploid origins with St, Y, and H haplome combinations in Elymus. Population genomic analyses indicate that E. nutans has expanded from medium to high/low-altitude regions. Phenotype/environmental association analyses identify MAPKKK18 promoter mutations reducing its expression, aiding UV-B adaptation in high-altitude populations. These findings enhance understanding of allopolyploid evolution and aid in breeding forage and cereal crops through intergeneric hybridization within Triticeae.