By providing new approaches to the investigation of demographic and evolutionary dynamics of wild populations, molecular genetics has led to fundamental changes in our understanding of marine ecology. In particular, genetic approaches have revolutionized our understanding in three areas: (i) most importantly, they have contributed to the discovery of extensive genetic population structure in many marine species, overturning the notion of large, essentially homogenous marine populations limiting local adaptation and speciation. (ii) Concomitant differences in ecologically important traits now indicate extensive adaptive differentiation and biocomplexity, potentially increasing the resilience to exploitation and disturbance. Evidence for rapid adaptive change in many populations underlies recent concerns about fisheries-induced evolution affecting life-history traits. (iii) A compilation of recent published research shows estimated effective population sizes that are 2–6 orders of magnitude smaller than census sizes, suggesting more complex recruitment dynamics in marine species than previously assumed. Studies on Atlantic cod are used to illustrate these paradigm shifts. In our synthesis, we emphasize the implications of these discoveries for marine ecology and evolution as well as the management and conservation of exploited marine fish populations. An important implication of genetic structuring and the potential for adaptive divergence is that locally adapted populations are unlikely to be replaced through immigration, with potentially detrimental consequences for the resilience to environmental change – a key consideration for sustainable fisheries management.