A global decline in seagrass populations has led to renewed calls for their conservation as important providers of biogenic and foraging habitat, shoreline stabilization and carbon storage. Eelgrass (Zostera marina) occupies the largest geographic range among seagrass species spanning a commensurately broad spectrum of environmental conditions. In Canada, eelgrass is managed as a single phylogroup despite occurring across three oceans and a range of ocean temperatures and salinity gradients. Previous research has focused on applying relatively few markers to reveal population structure of eelgrass, whereas a whole‐genome approach is warranted to investigate cryptic structure among populations inhabiting different ocean basins and localized environmental conditions. We used a pooled whole‐genome re‐sequencing approach to characterize population structure, gene flow and environmental associations of 23 eelgrass populations ranging from the Northeast United States to Atlantic, subarctic and Pacific Canada. We identified over 500,000 SNPs, which when mapped to a chromosome‐level genome assembly revealed six broad clades of eelgrass across the study area, with pairwise FST ranging from 0 among neighbouring populations to 0.54 between Pacific and Atlantic coasts. Genetic diversity was highest in the Pacific and lowest in the subarctic, consistent with colonization of the Arctic and Atlantic oceans from the Pacific less than 300 kya. Using redundancy analyses and two climate change projection scenarios, we found that subarctic populations are predicted to be potentially more vulnerable to climate change through genomic offset predictions. Conservation planning in Canada should thus ensure that representative populations from each identified clade are included within a national network so that latent genetic diversity is protected, and gene flow is maintained. Northern populations, in particular, may require additional mitigation measures given their potential susceptibility to a rapidly changing climate.