Many taxonomic groups contain both rare and widespread species, which indicates that range size can evolve quickly. Many studies have compared molecular genetic diversity, plasticity, or phenotypic traits between rare and widespread species; however, a suite of genetic attributes that unites rare species remains elusive. Here, using two rare and two widespread Boechera (Brassicaceae) species, we conduct a simultaneous comparison of quantitative trait diversity, genetic diversity, and population structure among species with highly divergent range sizes. Consistent with previous studies, we do not find strong associations between range size and within‐population genetic diversity. In contrast, we find that both the degree of phenotypic plasticity and quantitative trait structure ( Q ST) were positively correlated with range size. We also found higher F ST : Q ST ratios in rare species, indicative of either a greater response to stabilizing selection or a lack of additive genetic variation. While widespread species occupy more ecological and climactic space and have diverged at both traits and markers, rare species display constrained levels of population differentiation and phenotypic plasticity. Combined, our results provide evidence for a specialization–generalization trade‐off across three orders of magnitude of range size variation in the ecological model genus, Boechera.