These data were compiled to investigate the evolutionary history of Graham's beardtongue (Penstemon grahamii). Objective(s) of our study were to determine the evolutionary history of P. grahamii, including ancestral population sizes, the history of population divergences, and historical connectivity. In addition, we characterized population structure, genetic diversity summary statistics, and landscape factors influencing differentiation. These data represent anonymous loci sequenced from throughout the P. grahamii genome (specifically, .vcf and .structure files). Data in these files were manipulated to represent site frequency spectra between population pairs (.data files). These data were collected in 2019 from across the P. grahamii distribution, which is located in northeastern Utah and western Colorado. Specifically, plants are located at lower elevations on the northern slope of the Book Cliffs, which forms the southern side of the Uinta Basin. These data were collected by employees of the U.S. Geological Survey. Known occurrences of P. grahamii were visited and leaf samples from individual plants were collected from across the species’ distribution. These data can be used to further investigate the genetic differentiation, genetic diversity, and evolutionary history of P. grahamii.