Sustainable management of wheat stripe rust, caused by the fungus Puccinia striiformis Westend f. sp. tritici, and one of the most destructive wheat diseases can be achieved through the deployment of rust-resistant cultivars. In the frame of SusCrop-ERA-NET “WheatSustain” project, by incorporating state-of-the-art knowledge of host-pathogen relationships and validated QTL into models, we seek to improve the prediction accuracy of genomic selection (GS) for disease resistance in wheat. Our major goals in the present study were to identify the sources of effective resistance alleles and associated QTL for use in breeding programs and to evaluate marker assisted selection (MAS) and GS for stripe rust resistance in a diversity panel of 230 winter wheat from North and Central Europe. A genome-wide association study for adult plant stripe rust resistance identified 12 SNP markers on six wheat chromosomes which showed consistent effects over several testing environments. Among these, we found two marker loci on chromosomes 2BS (RAC875_c1226_652) and 6AL (Tdurum_contig29607_413) that were highly predictive in three independent validation populations of 1,065, 1,001, and 175 breeding lines. Lines showing the resistant haplotype at both loci were found nearly free of stripe rust symptoms. Using linear models with these markers as fixed effects, we could increase predictive ability in the three populations by 0.13-0.46 compared to a standard genomic best linear unbiased prediction approach. Our results demonstrate that, for the Northern and Central European winter wheat gene pool and current pathogen races, the two validated QTL on chromosomes 2B and 6A facilitate resistance through MAS and GS approaches. Understanding the genetic basis of stripe rust resistance aids the transfer of existing or new resistance alleles into high-yielding and regionally adapted lines in wheat breeding programs.