SignificancePerturbation of development often has nonrandom effects on trait expression. Such developmental bias is thought to constrain adaptation by making evolution more likely to proceed in certain directions. Developmental biases can evolve, but what role natural selection plays in this process remains highly controversial. Here, we estimate developmental bias in insect wings and show that it predicts variation among individuals, the effects of mutation, as well as deep macroevolutionary divergence that unfolded over ~60 My. This suggests that developmental biases can be strong predictors of diversification on both short and long evolutionary timescales but also challenges the classic view of strong relationships between genetic variation and divergence as solely reflecting constraints on adaptation.