Colonization of extreme habitats requires extensive adaptation to novel environmental challenges. Deep-water environments (>50 m) have high hydrostatic pressure, low temperature, and low light, requiring physiological and visual system adaptation, but genomic mechanisms underlying evolution in these environments are rarely known. Post-glacial colonization of Gander Lake in Newfoundland, Canada, by Arctic Charr (Salvelinus alpinus) provides the opportunity to study the genomic basis of adaptation to extreme deep-water environments. Here, we compare genomic and morphometric divergence between a phenotypically divergent deep-water, demersal morph adapted to depths of up to 288m and a larger, piscivorous morph occupying shallower depths. Using a SNP array and resequencing of nuclear and mitochondrial genomes, we find moderate genetic divergence (FST = 0.15 - 0.11) between morphs, consistent with divergence in body shape and size, despite absence of mitochondrial genome divergence. Outlier analyses identified three key genes with very high divergence against a genome-wide distribution of diverged genomic islands containing genes with functions related to deep-water adaptation such as sensory processes, ligand binding and regulation of transcription. Quantification of SNP array signal intensity variation associated with complex polymorphisms (e.g. copy number variants), similarly uncovered genetic separation of morphs and coincided with several islands of genomic divergence, but also revealed additional genomic regions and molecular mechanisms associated with depth adaptation. Together, these results show that adaptation to an extreme deep-water environment has been facilitated by multiple polymorphism types with roles in cellular and physiological processes, providing insight into the genomic basis of adaptation in extreme environments.