All biological populations are to a greater or lesser degree evolvable, but the forces that shape evolvability, especially the evolution of evolvability as an adaptive response to a changing environment, have been a source of controversy. One source of enhanced evolvability is the benign status of “cryptic sequences” typically expressed at low levels due to molecular errors, but with the potential to be expressed more fully following mutational co-option. A genome enriched for benign cryptic sequences has a more benign mutational neighborhood, via the possibility of co-option, and thus enhanced evolvability. Whether selection for evolvability itself can be the cause of a more benign mutational neighborhood remains an open question. Here, we show that environmental change can cause the evolution of increased evolvability, despite our use of a strong-selection weak mutation regime that precludes, by design, the adaptive evolution of evolvability. Instead, enhanced evolvability arises as a byproduct of environmental change via a novel mechanism that we call “emergent evolutionary capacitance”. When the environment changes, increased molecular error rates evolve as a strategy to rapidly change phenotypes, with the side effect of purging deleterious cryptic sequences and enhancing the mutational neighborhood for future adaptation. The behavior is strikingly similar to that seen in a model system for capacitance, the yeast prion [PSI+].