The non-genetic variation consists of phenotypic plasticity and developmental noise. Recent theoretical and empirical studies suggested that non-genetic variation may influence the direction and the rate of evolution, but the role of phenotypic plasticity and developmental noise are still poorly understood due to the difficulties in independently assessing the two components of non-genetic variation. Here, we estimated the ability of phenotypic plasticity and the degree of developmental noise in the wing shape and size of Drosophila simulans using a recently developed machine-learning based method. Both the degree of response to environmental changes (measurement of plasticity) and the degree of fluctuating asymmetry (measurement of developmental noise) for the shape and size of wings varied among isofemale lines derived from a single population, indicating genetic variation in the ability of phenotypic plasticity and the degree of developmental noise. We also found a positive relationship between the ability of phenotypic plasticity and the degree of developmental noise. These results suggest that the ability of phenotypic plasticity and the degree of developmental noise can themselves evolve and that these two components of non-genetic variation seem to influence the direction and the rate of evolution in a similar manner.