Winged bean (Psophocarpus tetragonolobus L.) is an underutilized legume of the family Fabaceae. We assembled 58,811 unigenes from the publicly available winged bean RNAseq data sets and discovered 4,107 perfect SSRs. Seventy-eight of the 166 SSRs amplified into a single band, of which 22 were polymorphic, in 79 germplasm accessions of winged bean constituting eight populations from India, Thailand, Nigeria, Indonesia, Taiwan, the Philippines, and Papua New Guinea. We found 60 alleles at the 22 polymorphic SSR loci, with a mean value of 2.73 per locus. With a mean of 0.36, the PIC values for the SSR loci ranged from 0.11 to 0.64. We recorded the maximum genetic diversity in advanced breeding lines (I = 0.67, He = 0.41) and the minimum genetic diversity in the germplasm accessions collected from Manipur (I = 0.44, He = 0.28), a north-eastern Indian state. The AMOVA analysis indicated that within-population variation was significantly higher (85%) than between-population variation (15%). The pairwise Nm values between the populations ranged between 0.69–3.41, indicating the varying level of gene flow between them. The analysis of the population structure based on the Bayesian model-based clustering algorithm revealed two distinct groups among the eight populations with different levels of introgression. The fuzzy clustering based on the Manhattan method also identified a similar number of groups, with 72% similarity between the two clustering methods. However, the Neighbour-Joining (NJ)-based clustering grouped all the accessions into four clusters. Nevertheless, all three clustering methods unanimously indicated that most African accessions tended to group, and their leftover members were spread across the hypothetical geographical populations, indirectly supporting the African origin of the winged bean.