The polar cod, Boreogadus saida, is an abundant and ubiquitous forage fish and a crucial link in Arctic marine trophic dynamics. Our objective was to unravel layers of genomic structure in B. saida from Canadian waters, specifically screening for potential hybridization with the Arctic cod, Arctogadus glacialis, large chromosomal inversions, and sex-linked regions, prior to interpreting population structure. Our analysis of 53,384 SNPs in 522 individuals revealed hybridization and introgression between A. glacialis and B. saida. Subsequent population level analyses of B. saida using 12,305 SNPs in 511 individuals revealed three large (ca. 7.4-16.1 Mbp) chromosomal inversions, and a 2 Mbp region featuring sex-linked loci. We showcase population structuring across the Western and Eastern North American Arctic, and subarctic regions ranging from the Hudson Bay to the Canadian Atlantic maritime provinces. Genomic signal for the inferred population structure was highly aggregated into a handful of SNPs (13.8%), pointing to potentially important adaptive evolution across the Canadian range. Our study provides a high-resolution perspective on the genomic structure of B. saida, providing a foundation for work that could be expanded to the entire circumpolar range for the species.