Many aspects of sensory information are linked in the natural environment, and evolution has shaped different navigational strategies across species to take advantage of this. A well-known example is celestial navigation in insects. Fruit flies use the position of the sun to navigate, but they can also orient successfully under the daytime sky even when the sun is not visible. This robustness is possible due to other global skylight cues—such as polarized light, spectral contrast, and intensity gradients—which all change in a stereotyped manner with respect to the position of the sun. Recent work in Drosophila shows that visual information about angles of polarized ultraviolet light (AOP) is conveyed to the central complex, the navigational center of the brain. However, the nature of how Drosophila use celestial cues to navigate is still not fully understood. Though the AOP pattern in the sky is used to infer a path that the observer and the sun lie on, it cannot provide information about which direction the sun lies on that path due to its symmetry. Thus, flies must integrate another asymmetrical skylight cue, such as the chromatic contrast gradient, to resolve this directional ambiguity. Using in vivo calcium imaging, we show chromatic tuning in ER4m, a visual ring neuron that is polarization sensitive and part of the celestial compass pathway. Specifically, ER4m is color opponent, i.e., inhibited by long wavelengths of light and excited by short wavelengths–a hallmark of chromatically tuned neurons. Furthermore, ER4m also responds to chromaticity contrast changes, where overall intensity is constant, in a distinct stepwise way. The appearance of polarization and chromatic information in ER4m demonstrate that these cues are integrated together before compass (E-PG) neurons, suggesting that chromatic information is used to resolve the AOP pattern’s directional ambiguity in the Drosophila celestial compass.