Peanut stem rot, also known as white mold, poses a significant threat to peanut production. It is typically managed using fungicides and moderately resistant cultivars. Cultivars with higher resistance can reduce fungicide dependency and increase sustainability. This study explores the potential of wild peanut species in stem rot resistance breeding programs by enhancing genetic diversity in cultivated peanut. Through greenhouse and field evaluations, 13 allotetraploid hybrids with Arachis stenosperma as one of the parents showed superior resistance compared to other wild genotypes. The genomic regions that confer the stem rot resistance were further identified by genotyping and phenotyping an F2 population derived from the allotetraploid ValSten1 (A. valida × A. stenosperma)4× and A. hypogaea cv. TifGP-2. A linkage map was constructed from 1926 SNP markers. QTL analysis revealed both beneficial and deleterious loci, with two resistance-associated QTLs derived from A. stenosperma and four susceptibility loci, two from A. stenosperma and two from A. valida. This is the first study that evaluated peanut-compatible wild-derived allotetraploids for stem rot resistance and that identified wild-derived QTLs for resistance to this pathogen. The allotetraploid hybrid ValSten1, that has A. stenosperma as one of the parents, offers a resource for resistance breeding. Markers associated with resistance QTLs can facilitate introgression from ValSten1 into cultivated peanut varieties in future breeding efforts, potentially reducing reliance on chemical control measures.