The SolCAP potato SNP array is a widely used tool for the rapid cost-effective genotyping of US tetraploid potatoes. When applied to the South American and European tetraploid collections, the array SNPs exhibit ascertainment bias. However, this ascertainment bias can be used as a tool to explore the relationship between South American, European, and US potatoes. In this study, we used 8296 SolCAP SNP markers on South American, European, and US potato populations intending to reveal the history of the three potato populations. We explored signatures of localized differentiation among the populations in order to identify potential loci under selection in potato history. Purging deleterious mutations were observed during major migration events. Admixtures and gene flow between potato populations were revealed. Furthermore, genome wide association mapping was conducted to uncover the genetic architecture of morphology in South American potato.