Preview: The effects of changing environments on phenotypic evolution are often studied in the context of climate and temperature change. However, changes in habitat structure and their associated light environments can also have substantial impacts on phenotypic evolution, especially for organisms that use color for intra- and interspecific signaling. According to the sensory drive hypothesis, adaptive signaling traits should use the colors that are most easily perceived in a given environmental context. However, such environments are likely to change as a result of anthropogenic activities, offering a powerful opportunity to test these predictions in natural populations. Using the Panamanian slender anole (Anolis apletophallus), which exhibits color polymorphism in its dewlap (categorized as a solid morph that is entirely orange and a bicolor morph that is mostly white with a small orange spot), we tested the relationship between morph frequencies and the light environment over nearly 40 years in a single population in Soberanía National Park, Panama. Our findings supported the sensory drive hypothesis, as dewlap morph frequencies were strongly correlated with light variables independently of neutral genetic structure. Moreover, we found surprisingly limited evidence that morphs differ in morphology, physiology, sperm characteristics, or behavior, suggesting that the historical stability and persistence of this color polymorphism over time may be primarily driven by the light environment. These results provide a framework for understanding the relative importance of factors that drive color evolution under changing light environments, especially as humans continue to alter habitat structure at unprecedented scales.