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Leaf rust, caused by the fungus Puccinia triticina Eriks (Pt), is a destructive disease affecting wheat (Triticum aestivum L.) production in many countries, and a serious threat to food security. As a result, several breeding programs have included leaf rust resistance as an important trait. The discovery and identification of new resistance genes that could aid in incorporating durable or long-lasting leaf rust resistance into wheat is fundamental in these breeding programs. The present study aimed to identify quantitative trait loci (QTLs) for leaf rust resistance in 127 recombinant inbred lines (RIL) developed from the cross between the resistant wheat cultivar Popo and the susceptible cultivar Kariega. The RIL population and parental lines were phenotyped for leaf rust infection type and severity at seedling and adult plant stage, respectively. The former in the greenhouse (in Argentina) and the latter in multiple field test environments comprising 3 locations in South Africa (in Tygerhoek in the Western Cape Province during the 2014, 2015, 2017 and 2018 cropping seasons; Clarens during 2014, 2016 and 2017 cropping seasons and in Bethlehem in the Free State Province during 2017 cropping season) and in 1 location in Argentina (during the 2017 and 2018 cropping seasons in Marcos Juárez, Córdoba Province). The population was genotyped using genotyping-by-sequencing. A total of 12,080 silicoDArT and 2,669 SNP markers were used for QTL analysis. In total, 25 putative QTLs for resistance to leaf rust at seedling and adult plant stages were identified, including 5 QTLs for seedling and 20 QTLs for adult plant resistance (APR). Interestingly, both Popo and Kariega contributed with alleles for resistance. Significant loci for reducing leaf rust infection at seedling stage were designated QLr.arc-1A, QLr.arc-2B, QLr.arc-5B, QLr.arc-6A and QLr.arc-6D. Three minor QTLs derived from Popo designated as QLr.arc-1B1, QLr.arc-2D and QLr.arc-3D were also detected from the field tests, explaining 5–10%, 10–16% and 5–7% of the phenotypic variance, respectively. The identified QTLs and their closely linked silicoDArT and SNP-based markers can be used for fine mapping and candidate gene discovery in wheat breeding programs targeting durable leaf rust resistance.