Light environments have a critical impact on species that use vision to survive and reproduce. Visual systems must accommodate changes in light that occur from minutes to years, yet we do not know how animal visual systems respond to spectral (color) changes over the longer time scales. Here we use an evolutionary experiment with different light environments to not only experimentally demonstrate that the visual system of guppies can evolve, but also show the effect of our evolutionary experiment on the plasticity of the visual system. We demonstrated changes in the visual system by examining the expression levels of nine guppy opsin genes; the genes that encode the light sensitive proteins in photoreceptors. In response to light, we found that some opsin expression levels underwent divergent evolution across generations and that the plastic response of a sub-set of opsin was determined by the light environment that the population evolved under.