Segregating alleles in natural populations can be driven to fixation or loss by genetic drift or directional selection, or may be maintained in a polymorphic state by balancing selection. Balancing selection in a panmictic population is theoretically well established, but not widely understood at the molecular level. In this study, we focus on the evolutionary processes affecting non-synonymous variants at eight functionally relevant loci (based on candidate SNP genotyping) in a deep-sea fish species (Coryphaenoides rupestris) that lives across habitat zones ranging from ~200 m to ~2000 m depth. At each of these loci, one allele is predominant in the deeper water. Across a shallower depth range, we find that minor allele frequencies show a highly significant increase or decline progressively across five defined age categories. At single depths below a threshold depth, the deep-water allele declines in frequency with age. Together, these data indicate segregatio n to different depths, either shallow or deep, and balancing selection to retain variants needed for each depth range. This is supported by signals for long-term balancing selection at these loci (based on published genomic data). We discuss alternative interpretations and conclude that balancing selection, maintaining ecotype diversity, is the best supported mechanism.