For colour vision, retinal circuits must separate information about intensity and wavelength. This requires circuit level comparison of at least two spectrally distinct photoreceptors. However, many vertebrates use four or more, and in those cases the nature and implementation of this computation remains poorly understood. Here, we establish the complete circuit architecture and function of outer retinal circuits underlying colour processing in the tetrachromatic larval zebrafish. Our findings reveal that the specific spectral tunings of the four cone types near optimally rotate the encoding of natural daylight in a principal component analysis (PCA)−like manner to yield one primary achromatic axis, two colour opponent axes as well as a secondary UV-achromatic axis for prey capture. We note that fruit flies − the only other tetrachromat species where comparable circuit-level information is available − use essentially the same strategy to extract spectral information from their relatively blue-shifted terrestrial visual world. Together, our results suggest that rotating colour space into achromatic and chromatic axes at the eye′s first synapse may be a fundamental principle of colour vision when using more than two spectrally well separated photoreceptor types.