Cowpea (Vigna unguiculata) is one of the major legume crops, widely distributed in tropical and subtropical regions of the world, and grown throughout China. Cowpea flower color is an important agronomic trait that plays an important role in its reproduction, but the molecular genetic basis of cowpea flower color variation is not known. To this end, this study used a combination of BSA-seq analysis based on flower color in a population of recombinant inbred lines (RILs) and genome-wide association analysis (GWAS) of flower color in a natural population of cowpea (271 accessions), which located the gene controlling flower color between 31.9 Mb and 32.3 Mb on chromosome IX (0.4 Mb region). The analysis showed that this 0.4-Mb region contains 30 genes, among which the TRANSPARENT TESTA GLABRA 1 (TTG1) gene is located near the peak of SNP-index and is involved in the regulation of anthocyanin biosynthesis in Arabidopsis. Further analysis using real-time fluorescence quantitative PCR (RT-PCR) revealed that there was a significant difference in gene expression of TTG1 between purple and white flag petals. In addition, two pairs of polymorphic SSR primers were screened within this region and were able to distinguish between purple and white flag petal individuals in the RIL population. The results of this study can provide some theoretical basis for cowpea flower color genetic variation and molecular breeding.