Background <p>Genome evolvability involves activation of transposable elements (TEs) that result in novel genomic rearrangements, including translocations, deletions, duplications, as well as larger structural reorganizations, such as chromosomal inversions and fusions. These genomic modifications contribute to raw genetic variability in which selection can act upon, and thus, promote local adaptation.</p> Results <p>Using a comparative genomics framework combined with the generation of six chromosome-level gadid reference genomes, including the cold-water adapted polar cod (<i>Boreogadus saida</i>) and Arctic cod (<i>Arctogadus glacialis</i>), we uncover an array of larger and smaller chromosomal reorganizations within this lineage. For the two Arctic codfishes, we detect lineage-specific chromosomal fusions, i.e., five in polar cod vs. eight in Arctic cod, resulting in a reduced number of chromosomes found to be associated with their geographical distribution. For the same species, we identify a high number of partly overlapping chromosomal inversions where a majority (especially within breakpoint regions) display an overrepresentation of specific TE families, accompanied by signatures of high degree of conservation. We further demonstrate involvement of miniature inverted-repeat transposable elements (MITEs) in the expansion of the well-known antifreeze glycoprotein genes in polar cod, and that the three gene clusters were localized in association with chromosomal rearrangements on chromosomes 1, 2, and 14.</p> Conclusions <p>We characterize how the Gadidae lineage has undergone massive genomic modifications — potentially via activation of TEs — throughout their evolutionary history, and particularly for the more Arctic species. These genomic reorganizations have likely played an important role in divergence processes and adaptation to freezing environmental conditions.</p>