Fish stocking has been utilized for over a century to offset extirpations or declines in abundance of many native species. These historical declines and hatchery contributions have led to uncertainty surrounding whether many contemporary populations are native, introgressed with hatchery sources, or entirely of hatchery origin. Such uncertainty is problematic for the conservation of native biodiversity as it hampers management agencies' ability to prioritize the conservation of indigenous locally adapted populations. Fortunately, genetic and genomic tools have allowed researchers to investigate these questions, often through the use of clustering or assignment approaches that are predicated on identifiable and consistent divergence between native populations and hatchery sources. Here, we apply these methods to restriction‐site associated DNA (RAD) data from 643 brook trout (Salvelinus fontinalis) originating from 13 wild populations and an exogenous hatchery strain to investigate the extent of historical extirpations, hatchery contributions, and processes affecting population structure in a small area of the previously unglaciated Driftless Area of Wisconsin, USA. The results from these analyses suggest that wild populations in this region are genetically distinct even at small spatial scales, lack strong hydrologically associated population structure, rarely exchange gene flow, and have small effective population sizes. Furthermore, wild populations are substantially diverged from known hatchery strains and show minimal evidence of introgression in clustering analyses. However, we demonstrate through empirically informed simulations that distinct wild populations may potentially be hatchery‐founded and have since diverged through rapid genetic drift. Collectively, the apparent lack of hydrological population structure and potential for rapid drift in the Driftless Area suggest that many native populations may have been historically extirpated and refounded by stocking events. If this is the case, then commonly used genomic clustering methods and their associated model selection criteria may result in underestimation of hatchery introgression in the face of rapid drift.