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Background Emerging wheat stem rust races have become a major threat to global wheat production. Finding additional loci responsible for resistance to these races and incorporating them into currently cultivated varieties is the most economic and environmentally sound strategy to combat this problem. Thus, this study was aimed at characterizing the genetic diversity and identifying the genetic loci conferring resistance to the stem rust of wheat. To accomplish this, 245 elite lines introduced from the International Center for Agricultural Research in the Dry Areas (ICARDA) were evaluated under natural stem rust pressure in the field at the Debre Zeit Agricultural Research Center, Ethiopia. The single nucleotide polymorphisms (SNP) marker data was retrieved from a 15 K SNP wheat array. A mixed linear model was used to investigate the association between SNP markers and the best linear unbiased prediction (BLUP) values of the stem rust coefficient of infection (CI). Results Phenotypic analysis revealed that 46% of the lines had a coefficient of infection (CI) in a range of 0 to 19. Genome-wide average values of 0.38, 0.20, and 0.71 were recorded for Nei’s gene diversity, polymorphism information content, and major allele frequency, respectively. A total of 46 marker-trait associations (MTAs) encompassed within eleven quantitative trait loci (QTL) were detected on chromosomes 1B, 3A, 3B, 4A, 4B, and 5A for CI. Two major QTLs with –log10 (p) ≥ 4 (EWYP1B.1 and EWYP1B.2) were discovered on chromosome 1B. Conclusions This study identified several novel markers associated with stem rust resistance in wheat with the potential to facilitate durable rust resistance development through marker-assisted selection. It is recommended that the resistant wheat genotypes identified in this study be used in the national wheat breeding programs to improve stem rust resistance.