Understanding the genetic basis of domestication-related traits (DRTs) is crucial for crop improvement. In this study, we developed an interspecific backcross population by crossing the elite cowpea variety Sam with a wild accession of Vigna unguiculata var. spontanea from Senegal. Using a mid-density single nucleotide polymorphism panel, we constructed a high-quality genetic linkage map consisting of 1,046 polymorphic markers spanning 1,131.6 cM across 11 chromosomes and used it as a framework for dissecting the genetic architecture of key DRTs. Over 2 consecutive years, we identified 65 quantitative trait loci (QTLs) associated with 17 key domestication traits, with 73.8% of these QTLs consistently detected across both years. Notably, we observed a significant clustering of domestication-related QTLs within 4 major genomic regions on chromosomes Vu01, Vu03, Vu08, and Vu09, particularly for organ size and phenological traits. The co-location of QTLs for traits such as pod shattering, growth habit, and flowering time suggests pleiotropy or potential co-selection of linked genes during domestication. Furthermore, our findings support the hypothesis of 2 independent domestication events in cowpea, as evidenced by similarities as well as differences in QTL regions between our study and previous reports. We hypothesized that common as well as different loci may have been selected during the 2 independent domestication events of cowpea, paralleling the dual domestication in common beans. While wild cowpea species contributed limited major-effect QTLs for yield-related traits, they remain an essential reservoir of genetic diversity, particularly for pest and disease resistance. These insights enhance our understanding of cowpea domestication and offer valuable genetic resources for breeding programs.