Evolutionary theory predicts that different selective regimes may contribute to divergent evolution of body size and growth rate among populations, but most studies have focused on allopatric populations. Here, we studied five sympatric subpopulations of anadromous northern pike (Esox lucius) in the Baltic Sea subjected to allopatric habitats for a short period of their life cycle due to homing behavior. We report differences in adult body size among subpopulations that were in part due to variation in growth rate. Body size of emigrating juveniles also differed among subpopulations, and differences remained when individuals were reared in a common environment, thus indicating evolutionary divergence among subpopulations. Furthermore, a QST-FST comparison indicated that differences had evolved due to divergent selection rather than genetic drift, possibly in response to differences in selective mortality among spawning habitats during the allopatric life stage. Adult and juvenile size were negatively correlated across subpopulations, and reconstruction of growth trajectories of adult fishes suggested that body size differences developed gradually and became accentuated throughout the first years of life. These results represent rare evidence that sympatric subpopulations can evolve differences in key life-history traits despite being subjected to allopatric habitats during only a very short fraction of their life.