Fusarium wilt is a vascular disease caused by the fungus Fusarium oxysporum f.sp. tracheiphilum (Fot) in cowpea [Vigna unguiculata (L.) Walp]. In this study, we mapped loci conferring resistance to Fot race 4 in three cowpea RIL populations: IT93K-503-1 × CB46, CB27 × 24-125B-1, and CB27 × IT82E-18/Big Buff. Two independent loci which confer resistance to Fot race 4 were identified, Fot4-1 and Fot4-2. Fot4-1 was identified in the IT93K-503-1 (resistant) × CB46 (susceptible) population and was positioned on the cowpea consensus genetic map, spanning 21.57-29.40 cM on linkage group 5. The Fot4-2 locus was validated by identifying it in both the CB27 (resistant) × 24-125B-1 (susceptible) and CB27 (resistant) × IT82E-18/Big Buff (susceptible) populations. Fot4-2 was positioned on the cowpea consensus genetic map on linkage group 3; the minimum distance spanned 71.52-71.75 cM whereas the maximum distance spanned 64.44-80.23 cM. These genomic locations of Fot4-1 and Fot4-2 on the cowpea consensus genetic map, relative to Fot3-1 which was previously identified as the locus conferring resistance to Fot race 3, established that all three loci were independent. The Fot4-1 and Fot4-2 syntenic loci were examined in Glycine max, where several disease-resistance candidate genes were identified for both loci. In addition, Fot4-1 and Fot4-2 were coarsely positioned on the cowpea physical map. Fot4-1 and Fot4-2 will contribute to molecular marker development for future use in marker-assisted selection, thereby expediting introgression of Fot race 4 resistance into future cowpea cultivars.