Comparisons of estimates of genetic differentiation at molecular markers (F_ST) and at quantitative traits (Q_ST) are a means of inferring the level and heterogeneity of selection in natural populations. However, such comparisons are questionable because they require that the influence of drift and selection on Q_ST be detectable over possible background influences of environmental or nonadditive genetic effects on Q_ST-values. Here we test this using an experimental evolution approach in metapopulations of Arabidopsis thaliana experiencing different levels of drift and selection heterogeneity. We estimated the intensity and heterogeneity of selection on morphological and phenological traits via selection differentials. We demonstrate that Q_ST-values increased with increasing selection heterogeneity when genetic drift was limited. The effect of selection on Q_ST was thus detectable despite significant genotype-by-environment interactions that most probably biased the estimates of genetic differentiation. Although they cannot be used as a direct validation of the conclusions of prior studies, our results strongly support both the relevance of Q_ST as an estimator of genetic differentiation and the role of local selection in shaping the genetic differentiation of natural populations.