Penstemon × jonesii is described as having flowers with the colors of “Tyrian rose,” “amaranth purple,” or “red-purple to maroon.” It has been recorded only in localized areas of southwestern Utah and just over the border of Arizona, where both putative parents commonly occur in sandy soils. Penstemon × jonesii has been reported and widely accepted as a natural hybrid of P. laevis × P. eatonii, though no research has been conducted to verify this assumption. We examined claims of its hybrid origin by making interspecific reciprocal first-generation hybrid plants from the 2 suspected parental species (P. eatonii and P. laevis) as well as by making second-generation hybrids through backcrossing to both parental species. Using 9 Penstemon simple sequence repeat (SSR), or microsatellite, markers, we examined the allelic variation among natural populations of P. × jonesii, P. eatonii, and P. laevis in southwestern Utah. These SSR data, in conjunction with our controlled crosses, support claims that P. × jonesii likely descends from hybridization events between P. eatonii and P. laevis. Flower color of the typical P. × jonesii reported in the literature and found in herbarium samples does not resemble the flower color of F₁P. eatonii × P. laevis hybrids from our controlled crosses. However, in subsequent controlled backcrossing of the F₁ hybrids to P. eatonii, we found blossom morphotypes and corolla colors matching previous descriptions of P. × jonesii. We also observed many hybrids with lighter corolla colors, such as light pinks, pinkish yellows, and lavender, which are not recorded in the literature or found in herbarium specimens. Field surveys for natural color variation in P. × jonesii populations also revealed greater flower color variation than previously reported, which should be considered as part of this hybrid taxa as well, though the predominant floral colors of P. × jonesii are “Tyrian rose,” “amaranth purple,” and “red-purple to maroon,” which suggests some selective bias. We suggest that pollinator preference for dark red to purple blooms may be responsible for this phenomenon.