AbstractSpecies at the periphery of their range are typically limited in density by poor habitat quality. As a result, the central–marginal hypothesis (CMH) predicts a decline in genetic diversity of populations toward the periphery of a species' range. Grizzly bears (Ursus arctos) once ranged throughout most of North America but have been extirpated from nearly half of their former range, mainly in the south. They are considered a species at risk even in Canada's remote North, where they occupy the northernmost edge of the species' continental distribution in a low‐productivity tundra environment. With climate change, one of their main prey species in the tundra (caribou), which has always shown yearly fluctuations, is declining, but simultaneously, grizzlies appear to be expanding their range northward in the same tundra environment. Yet, a lack of population density estimates across the North is hindering effective conservation action. The CMH has implications for the viability of peripheral populations, and the links between population fluctuations, potential bottlenecks, and genetic diversity need to be determined to contribute to species' conservation. Using noninvasive genetic sampling from 2012 to 2014 and autosomal DNA genotyping (via microsatellites), we estimated bear density using a spatial capture–recapture framework and analyzed genetic diversity using observed heterozygosity (Ho), allelic richness (AR), and expected heterozygosity (He). We compared our findings to other studies that used comparable methodologies on grizzly bears and a related species (black bears; Ursus americanus). We found densities of grizzly bears that were low for the species but characteristic for the region (5.9 ± 0.4 bears/1000 km2), but with high Ho (0.81 ± 0.05), AR (7 ± 0.78), and He (0.71 ± 0.03), despite a signal of recent bottlenecks. In both species, peripherality was not correlated with Ho but was negatively correlated with density. We suggest that the apparent growth of this expanding population of grizzlies offsets the negative impacts of recent bottlenecks on Ho. Indigenous knowledge provides historical context (on the order of centuries, e.g., arctic large mammal fluctuations, grizzly bear bottlenecks) for the current bear population dynamics (on the order of decades, e.g., climate change, northern grizzly bear expansion).