Stripe rust, caused by Puccinia striiformis f. sp. tritici (Pst), is one of the most damaging diseases of wheat globally and resistance is the effectively control strategy. Triticum boeoticum Boiss (T. monococcum L. ssp. aegilopoides, 2n = 2x = 14, AbAb) accession G52 confers a high level of adult-plant resistance against a mixture of the Chinese prevalent Pst races. To transfer the resistance to common wheat, a cross was made between G52 and susceptible common wheat genotype Crocus. A highly resistant wheat-T. boeoticum introgression line Z15-1370 (F5 generation) with 42 chromosomes was selected cytologically and by testing with Pst races. In order to map the resistance gene(s), F1, F2, and F2:3 generations of the cross between Z15-1370 and stripe rust susceptible common wheat Mingxian169 were developed. Genetic analysis revealed that the resistance in Z15-1370 was controlled by a single recessive gene, temporarily designated YrZ15-1370. Using the bulked segregant RNA-Seq (BSR-Seq) analysis, YrZ15-1370 was mapped to chromosome 6AL and flanked by markers KASP1370-3 and KASP-1370-5 within a 4.3 cM genetic interval corresponding to 1.8 Mb physical region in the Chinese Spring genome, in which a number of disease resistance-related genes were annotated. YrZ15-1370 differed from previously Yr genes identified on chromosome 6A based on its position and/or origin. The YrZ15-1370 would be a valuable resource for wheat resistance improvement and the flanking markers developed here should be useful tools for marker-assisted selection (MAS) in breeding and further cloning the gene.