Maintenance of a portfolio of adaptive alleles may provide resilience of populations to natural environmental variability. We used Pacific ocean perch (POP; Sebastes alutus) to test for the maintenance of adaptive variation across overlapping generations. POP are a long-lived species characterized by widespread larval dispersal in their first year and a longevity of over 100 years. In order to understand how early marine dispersal affects POP survival and population structure, we used Restriction Site Associated DNA sequencing (RADseq) to obtain 11,146 single-nucleotide polymorphisms (SNPs) from 401 young-of-the-year (YOY) POP collected during surveys conducted in 2014 (19 stations) and 2015 (4 stations) in the eastern Gulf of Alaska. Population clustering analysis showed that the POP samples represented four distinct ancestral populations mixed throughout the sampling area. Based on prior work on larval dispersal of POP, these larvae are most likely from distinct parturition locations that are mixing during their pelagic dispersal life stage. Latent factor mixed models revealed that POP larvae face significant selection during their first year at sea, which were specific to the year of their birth. Thus each adult cohort’s genetic composition is heavily influenced by the environmental conditions experienced during their first year at sea. Long-lived species relying on broadcast spawning strategies may therefore be uniquely resilient to environmental variability by maintaining a portfolio of cohort-specific adaptive genotypes, and age truncation due to overfishing of older cohorts may have detrimental effect on the population viability.