A high degree of trophic polymorphism has been associated with the absence of high variability in population density. An explanation for this pattern is that density fluctuations may influence selective regime forms in populations. Still, only few studies have investigated evolutionary dynamics in fluctuating populations. Here we report on a multiyear study of the Eurasian perch, wherein the fitness landscape shifts between stabilizing and directional selection at low density to disruptive selection at high density. Intrinsically driven population fluctuations is the mechanism that most likely explains these shifts in fitness landscape. Stable isotope data showed that the habitat choices of perch were stable over the growing season, indicating that the selection pressure observed each year influenced the fitness of perch in the following year's reproductive period. Furthermore, the morphological differences between perch caught in the two habitats (littoral and pelagic) were more pronounced at high density than at low density. This study shows that an explicit consideration of population dynamics may be essential to explain the long-term evolutionary dynamics in populations. In particular, fluctuating population dynamics may be one explanation for why not all polymorphic populations lead to speciation. Instead, fluctuating population dynamics may favor the evolution of phenotypic plasticity.