While Atlantic salmon (Salmo salar) of the northernmost American populations is alimentary, economically, and culturally important for Ungava Inuit communities (Nunavik, Canada) and might play a key role in the persistence of the species in a global warming context, many mysteries remain about those remote and atypical populations. Thus, our first aim was to document the genomic structure of the Nunavik populations. The second objective was to determine whether salmon only migrating to the estuary without reaching the sea, apparently unique to those populations, represent distinct populations from the typical anadromous salmons and subsequently explore the genetic basis of migratory life‐history tactics in the species. Finally, the third goal was to quantify the contribution of each genetically distinct population and life‐history tactic in the mixed‐stock subsistence fishery of the Koksoak R. estuary. We used Genotyping‐by‐Sequencing to genotype 14,061 single nucleotide polymorphisms in the genome of 248 individuals from 8 source populations and 280 individuals from the Koksoak estuary mixed‐stock fishery. Life‐history tactics were identified by a visual assessment of scales. Results show a hierarchical structure mainly influenced by isolation‐by‐distance with 7 populations out of the 8 studied rivers. While no obvious structure was detected between marine and estuarine salmon within the population, we have identified genomic regions putatively associated with those migration tactics. Finally, all salmon captured in the Koksoak estuary originated from the Koksoak drainage and mostly from 2 tributaries, but no inter‐annual variation in the contribution of these tributaries was found. Our results indicate, however, that both marine and estuarine salmon contribute substantially to estuarine fisheries and that there is inter‐annual variation in this contribution. These findings provide crucial information for the conservation of salmon populations in a rapidly changing ecosystem, as well as for fishery management to improve the food security of Inuit communities.