<p>Maintaining the adaptive capacity of wildlife populations facing rapid environmental change requires understanding the processes that erode genetic diversity. Effective population size governs the rate at which genetic diversity is lost to drift and the efficiency of natural selection, making it an important metric for assessing long-term population viability. Here, we use whole-genome resequencing of 140 beluga whales (<i>Delphinapterus leucas</i>) sampled across their eastern Canadian range to reconstruct demographic histories spanning one million years and estimate contemporary effective population sizes across six genetically distinct populations. Effective population size trajectories were shared until approximately 50,000 years ago, after which they began to separate in association with glacial dynamics and post-glacial colonization. These historical processes are reflected in contemporary genomic patterns, including pronounced variation in inbreeding, with the St. Lawrence Estuary population showing extensive runs of homozygosity consistent with long-term isolation that predates recent exploitation. Over the past millennium, population trajectories diverged further, with some populations increasing and others declining, in part reflecting known harvest histories. Contemporary effective population sizes exceed 2,000 in only two populations and fall below 400 in all others. Notably, populations with large census sizes sometimes exhibited low effective population sizes, indicating that apparent demographic stability may obscure reduced adaptive capacity. Our results demonstrate that beluga populations differ substantially in their evolutionary histories and current genetic health, such that whole species-level conservation and management may overlook important variation in vulnerability to future environmental change.</p>