Most yeast genes are dispensable for optimal growth in laboratory cultures. However, this apparent lack of fitness contribution is difficult to reconcile with the theory of natural selection. Here we use stochastic modeling to show that environmental fluctuations can select for a genetic mechanism that does not affect growth in static laboratory environments. We then present a novel experimental platform for measuring the fitness levels of specific genotypes in fluctuating environments. We test this platform by monitoring a mixed culture of two yeast strains that differ in their ability to respond to changes in carbon source yet exhibit the same fitness level in static conditions. When the sugar in the growth medium was switched between galactose and glucose, the wild-type strain gained a growth advantage over the mutant strain. Interestingly, both our computational and experimental results show that the strength of the adaptive advantage conveyed by the wild-type genotype depends on the total number of carbon source switches, not on the frequency of these fluctuations. Our results illustrate the selective power of environmental fluctuations on seemingly slight phenotypic differences in cellular response dynamics and underscore the importance of dynamic processes in the evolution of species.