Trait diversity – the substrate for natural selection – is necessary for adaptation through selection, particularly in populations faced with environmental changes that diminish population fitness. In habitats that remain unchanged for many generations, stabilizing selection maximizes exploitation of resources by reducing trait diversity to a narrow optimal range. One might expect that such ostensibly homogeneous populations would have a reduced potential for heritable adaptive responses when faced with fitness-reducing environmental changes. However, field studies have documented populations that, even after long periods of evolutionary stasis, can still rapidly evolve in response to changed environmental conditions. We argue that degeneracy, the ability of diverse population elements to function similarly, can satisfy both the current need to maximize fitness and the future need for diversity. Degenerate ensembles appear functionally redundant in certain environmental contexts and functionally diverse in others. We propose that genetic variation not contributing to the observed range of phenotypes in a current population, also known as cryptic genetic variation (CGV), is a specific case of degeneracy. We argue that CGV, which gradually accumulates in static populations in stable environments, reveals hidden trait differences when environments change. By allowing CGV accumulation, static populations prepare themselves for future rapid adaptations to environmental novelty. A greater appreciation of degeneracy’s role in resolving the inherent tension between current stabilizing selection and future directional selection has implications in conservation biology and may be applied in social and technological systems to maximize current performance while strengthening the potential for future changes.