The species Vigna unguiculata L. (Walp), commonly known as cowpea, is a multi-purpose legume that has been selected into three subspecies that are divided into grain, fodder and pod (yardlong bean) types. However, genetic bases for distinctions are not well understood. The purpose of this study was to apply genotyping-by-sequencing (GBS) and current reference genome for V. unguiculata to distinguish three subspecies and identify signatures of divergence. The collection of 130 accessions included 128 cultivated from: 1) ssp. cylindrica, fodder type, 2) ssp. sesquipedalis, pod vegetable type, and 3) ssp. unguiculata, grain type. Two wilds genotypes from spp. dekindtiana and spp. pubescens, were used to anchor phylogeny. A total of 11,083 highly informative single nucleotide polymorphisms (SNPs) were discovered. Wild accessions showed distinct genetic fingerprints and were separated from cultivated subspecies. Principal component analysis showed closer relationship between ssp. unguiculata and ssp. cylindrica compared to ssp. sesquipedalis. Relative differentiation of cultivated subspecies (with Fixation Index, FST) indicated the existence of discrete signatures of selection. This work clarifies the population structure, phylogeny, and domestication of cultivated cowpeas. Furthermore, significant genetic differences between grain and pod vegetable types can provide valuable information for future breeding in three cowpea groups.