Chromosome structural variation may underpin ecologically-important intraspecific diversity by reducing recombination within supergenes containing linked, co-adapted alleles. Here, we confirm that an ancient chromosomal rearrangement is strongly associated with migratory phenotype and individual genetic structure in Atlantic cod (Gadus morhua) across the Northwest Atlantic. We reconstruct trends in effective population size over the last century, and for the first time reveal declines in effective population size matching onset of industrialized harvest (post 1950). We find different demographic trajectories between individuals homozygous for the chromosomal rearrangement relative to heterozygous or homozygous individuals for the non-inverted haplotype, suggesting different selective histories across the last 150 years. These results illustrate how chromosomal structural diversity can mediate fine-scale genetic, phenotypic and demographic variation in a highly connected marine species, and show how overfishing may have led to loss of biocomplexity within Northern cod.