Functional connectivity (i.e., the movement of individuals across a landscape) is essential for the maintenance of genetic variation and persistence of rare species. However, illuminating the processes influencing functional connectivity and ultimately translating this knowledge into management practice remains a fundamental challenge. Here, we combine various population structure analyses with pairwise, population-specific demographic modeling to investigate historical functional connectivity in Graham’s beardtongue (Penstemon grahamii), a rare plant narrowly distributed across a dryland region of the western US. While principal component and population structure analyses indicated an isolation-by-distance pattern of differentiation across the species’ range, spatial inferences of effective migration exposed an abrupt shift in population ancestry near the range center. To understand these seemingly conflicting patterns, we tested various models of historical gene flow and found evidence for recent admixture (~ 3400 generations ago) between populations near the range center. This historical perspective reconciles population structure patterns and suggests management efforts should focus on maintaining connectivity between these previously isolated lineages to promote the ongoing transfer of genetic variation. Beyond providing species-specific knowledge to inform management options, our study highlights how understanding demographic history may be critical to guide conservation efforts when interpreting population genetic patterns and inferring functional connectivity.