Robustness against environmental fluctuations within an adaptive state should preclude exploration of new adaptive states when the environment changes. Here, we study transitions between adaptive associations of feather structure and carotenoid uptake to understand how robustness and evolvability can be reconciled. We show that feather modifications induced by unfamiliar carotenoids during a range expansion are repeatedly converted into precise coadaptations of feather development and carotenoid accommodation as populations persist in a region. We find that this conversion is underlain by a uniform and coordinated increase in the sensitivity of feather development to local carotenoid uptake, indicative of cooption and modification of the homeostatic mechanism that buffers feather growth in the evolution of new adaptations. Stress-buffering mechanisms are well placed to alternate between robustness and evolvability and we suggest that this is particularly evident in adaptations that require close integration between widely fluctuating external inputs and intricate internal structures.