The evolution of flapping flight is linked to the prolific success of insects. Across Insecta, wing morphology diversified, strongly impacting aerodynamic performance. In the presence of ecological opportunity, discrete adaptive shifts and early bursts are two processes hypothesized to give rise to exceptional morphological diversification. Here, we use the sister-families Sphingidae and Saturniidae to answer how the evolution of aerodynamically important traits is linked to clade divergence and through what process(es) these traits evolve. Many agile Sphingidae evolved hover feeding behaviours, while adult Saturniidae lack functional mouth parts and rely on a fixed energy budget as adults. We find that Sphingidae underwent an adaptive shift in wing morphology coincident with life history and behaviour divergence, evolving small high aspect ratio wings advantageous for power reduction that can be moved at high frequencies, beneficial for flight control. By contrast, Saturniidae, which do not feed as adults, evolved large wings and morphology which surprisingly does not reduce aerodynamic power, but could contribute to their erratic flight behaviour, aiding in predator avoidance. We suggest that after the evolution of flapping flight, diversification of wing morphology can be potentiated by adaptative shifts, shaping the diversity of wing morphology across insects.