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Rare species of plants are especially vulnerable to extinction when populations are few, have small numbers of individuals, and are fragmented. Such conditions lead to a reduction in gene flow and genetic diversity, and encourage inbreeding depression. We conducted a study of the reproductive biology and population genetics of Penstemon debilis (Plantaginaceae), a Federally Threatened species endemic to a small region of oil shale extraction in western Colorado, USA. Most of the habitat area is privately owned and undergoing natural gas extraction activities. Penstemon debilis reproduces both vegetatively and as an outcrosser that requires a pollen vector. Moderate levels of inbreeding, but no inbreeding depression, were found within populations of P. debilis. Genetic divergence among the extant populations surveyed was moderate (FST values = 0.069–0.231; Nm = 0.831–3.385) with levels of genetic diversity within populations relatively low compared to congeners with similar modes of pollination and reproductive biology. STRUCTURE analysis revealed three population clusters with some admixture among all extant populations. Genetic diversity within and among P. debilis populations is similar to genetic diversity found for other rare and endemic outcrossing plant species. Our results are consistent with a pattern of recent population fragmentation or low levels of pollen‐mediated gene flow among populations in close proximity to one another. Conservation of P. debilis will require cooperative management strategies between private landowners, government agencies, and concerned NGOs to preserve habitat for this rare species.