The allotetraploid wild grass Aegilops ventricosa (2n = 4x = 28, genome DvDvNvNv) has been recognized as an important germplasm resource for wheat improvement owing to its ability to tolerate biotic stresses. In particular, the 2NvS segment from Ae. ventricosa, as a stable and effective resistance source, has contributed greatly to wheat improvement. The 2NvS/2AS translocation is a prevalent chromosomal translocation between common wheat and wild relatives, ranking just behind the 1B/1R translocation in importance for modern wheat breeding. Here, we assembled a high-quality chromosome-level reference genome of Ae. ventricosa RM271 with a total length of 8.67 Gb. Phylogenomic analyses revealed that the progenitor of the Dv subgenome of Ae. ventricosa is Ae. tauschii ssp. tauschii (genome DD); by contrast, the progenitor of the D subgenome of bread wheat (Triticum aestivum L.) is Ae. tauschii ssp. strangulata (genome DD). The oldest polyploidization time of Ae. ventricosa occurred ∼0.7 mya. The Dv subgenome of Ae. ventricosa is less conserved than the D subgenome of bread wheat. Construction of a graph-based pangenome of 2AS/6NvL (originally known as 2NvS) segments from Ae. ventricosa and other genomes in the Triticeae enabled us to identify candidate resistance genes sourced from Ae. ventricosa. We identified 12 nonredundant introgressed segments from the Dv and Nv subgenomes using a large winter wheat collection representing the full diversity of the European wheat genetic pool, and 29.40% of European wheat varieties inherit at least one of these segments. The high-quality RM271 reference genome will provide a basis for cloning key genes, including the Yr17-Lr37-Sr38-Cre5 resistance gene cluster in Ae. ventricosa, and facilitate the full use of elite wild genetic resources to accelerate wheat improvement.