Although adaptive plasticity would seem always to be favored by selection, it occurs less often than expected. This lack of ubiquity suggests that there must be trade-offs, costs, or limitations associated with plasticity. Yet, few costs have been found. We explore one type of limitation, a correlation between plasticity and developmental instability, and use quantitative genetic theory to show why one should expect a genetic correlation. We test that hypothesis using the Landsberg erecta × Cape Verde Islands recombinant inbred lines (RILs) of Arabidopsis thaliana. RILs were grown at four different nitrogen (N) supply levels that span the range of N availabilities previously documented in North American field populations. We found a significant multivariate relationship between the cross-environment trait plasticity and the within-environment, within-RIL developmental instability across 13 traits. This genetic covariation between plasticity and developmental instability has two costs. First, theory predicts diminished fitness for highly plastic lines under stabilizing selection, because their developmental instability and variance around the optimum phenotype will be greater compared to nonplastic genotypes. Second, empirically the most plastic traits exhibited heritabilities reduced by 57% on average compared to nonplastic traits. This demonstration of potential costs in inclusive fitness and heritability provoke a rethinking of the evolutionary role of plasticity.