Understanding the relationship between census size, recent demography and genetic diversity is central for effective conservation and management of threatened species. Thorny skate (Amblyraja radiata) biomass in the northwest Atlantic has declined significantly in the past 50 years, prompting strict conservation measures . Curiously, population recovery has not occurred in the Gulf of Maine. We conducted whole genome sequencing of thorny skate samples collected from across its range. Genetic diversity was similar in all sampled locations, but we discovered a ~31 megabase supergene bi-allelic locus associated with a discrete size polymorphism occurring in the northwest Atlantic. Historical demographic modelling reveals that the allele associated with larger size originally introgressed into the ancestral thorny skate population ~160,000 years ago. Off Newfoundland (Canada), where population recovered, supergene genotypes are in Hardy-Weinberg equilibrium. In contrast, the Gulf of Maine population, exhibiting the most acute non-recovery, displays a significant deficit of heterozygotes. This strongly implies sub-regional fitness effects associated with the supergene, hindering recovery efforts in the Gulf of Maine. At the same time, regional migration sustains genetic variability in the recombining genome component, preventing speciation between morphs. This study highlights a rarely considered significance of context-dependent genetic compatibilities in the conservation of threatened populations and reconcile census size trajectory with genetic diversity estimates through accurate evolutionary modelling.