The two recombinant inbred line (RIL) populations developed by crossing Almaly × Avocet S (206 RILs) and Almaly × Anza (162 RILs) were used to detect the novel genomic regions associated with adult plant resistance (APR) and seedling or all-stage resistance (ASR) to yellow rust (YR) and leaf rust (LR). The quantitative trait loci (QTLs) were detected through multi-year phenotypic evaluations (2018–2020) and using high-throughput DArTseq genotyping technology. RILs exhibited significant genetic variation with p < 0.001, and the coefficient of variation ranged from 9.79% to 47.99% for both LR and YR in all Environments and stages of evaluations. The heritability is quite high and ranged between 0.47 and 0.98. We identified nine stable QTLs for YR APR on chromosomes 1B, 2A, 2B, 3D, and 4D and four stable QTLs for LR APR on chromosomes 2B, 3B, 4A, and 5A. Furthermore, in silico analysis revealed that the key putative candidate genes such as cytochrome P450, protein kinase-like domain superfamily, zinc-binding ribosomal protein, SANT/Myb domain, WRKY transcription factor, nucleotide sugar transporter, and NAC domain superfamily were in the QTL regions and probably involved in the regulation of host response toward pathogen infection. The stable QTLs identified in this study are useful for developing rust-resistant varieties through marker-assisted selection (MAS).