Evolutionary changes in functional traits represent one possible reason why exotic species spread to become invasive, but empirical studies of the mechanisms driving phenotypic differentiation between populations of invasive species are rare. This study tested whether differences in distal spine length among populations of the invasive cladoceran, Bythotrephes longimanus, could be explained by local adaptation or phenotypic plasticity. We collected Bythotrephes from six lakes and found that distal spine lengths and natural selection on distal spine length differed among populations, but were unrelated to the gape-limitation of the dominant fish predator in the lake from which they were collected. A common garden experiment revealed significant genetic and maternal variation for distal spine length, but phenotypic differences among populations were not genetically based. Phenotypic differences among lakes in this ecologically important trait are, therefore, the result of plasticity and not local adaptation, despite spatially variable selection on this heritable trait. The ability of Bythotrephes to plastically adjust distal spine length may explain the success of this species at invading lake ecosystems with diverse biotic environments.