Color vision is widespread in the animal kingdom, and describes the ability to discriminate between objects purely based on the wavelengths that they reflect. Experiments across many species have isolated wavelength comparison in the brain as a computation underlying color vision. This comparison takes place in color opponent neurons, which respond with opposite polarity to wavelengths in different parts of the spectrum. In this work, I explore color opponency in the genetically tractable organism Drosophila melanogaster, where these circuits have only just begun to be described. Using two-photon calcium imaging, I measure the spectral tuning of photoreceptors in the fruit fly and identify circuit mechanisms that give rise to opponency. I find two pathways: an insect-specific pathway that compares wavelengths at each point in space, and a horizontal-cell-mediated pathway similar to that found in mammals. The horizontal-cell-mediated pathway enables additional spectral comparisons through lateral inhibition, expanding the range of chromatic encoding in the fly. Together, these two pathways enable efficient decorrelation and dimensionality reduction of photoreceptor signals while retaining maximal chromatic information. This dual mechanism combines motifs of both an insect-specific visual circuit and an evolutionarily convergent circuit architecture, endowing flies with the ability to extract chromatic information at distinct spatial resolutions.