Determining the degree to which variation in traits is controlled by genetics and/or environment is fundamental to understanding adaptation. In this study, we examine the genetic and environmental influences on color pattern expression in male bluefin killifish, Lucania goodei. This is a compelling system because both male color patterns and vision physiology are correlated with basic properties of the environment. Across populations, males with blue anal fins are more abundant in waters with low transmission of UV and blue wavelengths. Here, we present results from two paternal half-sib breeding experiments (one in the laboratory, one in the greenhouse) in which offspring were raised under light treatments that mimicked natural variation in the spectral composition of light. In both experiments, we found that red-versus-yellow expression is controlled by an autosomal locus of large effect where yellow (Y) is dominant over red (y). There was little blue expression in the laboratory. In the greenhouse, we found higher expression of blue anal fin morphs when males were raised in tea-stained water (low transmission UV/ blue) than when raised in clear water (high transmission UV/blue). We also found genetic effects of sires and an interaction between sire and lighting environment (i.e. heritable plasticity). These results show that a relatively simple, environmentally dependent, epistatic interaction can produce a large amount of variation in male color patterns that presumably function in sexual selection.