Ecotype variation in species exhibiting different life history strategies may reflect heritable adaptations to optimize reproductive success, and potential for speciation. Traditionally, ecotypes have, however, been defined by morphometrics and life history characteristics, which may be confounded with individual plasticity. Here, we use the widely distributed and polytypic freshwater fish species brown trout (Salmo trutta) as a model to study piscivorous life history and its genetic characteristics in environmentally contrasting habitats; a large lake ecosystem with one major large and stable tributary, and several small tributaries. Data from 550 fish and 13 polymorphic microsatellites (H e = 0.67) indicated ecotype‐specific genetic differentiation (θ = 0.0170, p < .0001) among Bayesian assigned small riverine resident and large, lake migrating brown trout (>35 cm), but only in the large tributary. In contrast, large trout did not constitute a distinct genetic group in small tributaries, or across riverine sites. Whereas life history data suggest a small, river resident and a large migratory piscivorous ecotype in all studied tributaries, genetic data indicated that a genetically distinct piscivorous ecotype is more likely to evolve in the large and relatively more stable river habitat. In the smaller tributaries, ecotypes apparently resulted from individual plasticity. Whether different life histories and ecotypes result from individual plasticity or define different genetic types, have important consequence for conservation strategies.