1 Abstract Evolutionary theory suggests that phenotypic stasis is explained by natural selection and genetic drift, or by constraints imposed by mutation and recombination of standing genetic variation. We performed experimental evolution from standing genetic variation with the nematode Caenorhabditis elegans , measuring individual locomotion in outcrossing populations for 240 generations. We find that, in our constant environment, locomotion bias shows no directional divergence, due to both stabilizing and disruptive selection on specific combinations of component traits. Despite phenotypic stasis, the genetic variance-covariance structure between component traits shows clear divergence from the ancestral state and extensive differentiation among replicated populations facing the same environment. Analysis of mutation accumulation experiments and genome-sequenced recombinant inbred lines from the experimental populations indicates that the evolution of the genetic variance-covariance structure is independent of de novo mutation or major effect QTL; being instead explained by the joint action of selection and drift in generating subtle linkage disequilibrium differences between small effect QTL among replicate populations. These findings indicate that phenotypic evolution is repeatable because of selection, even if the genetic structuring of component traits within lineages is mostly contingent upon drift history.