Significance Pigment–light interactions have shaped animal evolution, from vision to camouflage. How organisms cope with harmful photodegradative products while maintaining pigment-bearing cell integrity, from skin to light screening in eyes, remains mysterious. We studied color-changing crab spiders to unravel the intracellular mechanisms leading to within-cell formation and degradation of pigment organelles. We found that they belong to the widespread lysosome-related organelle family, like vertebrate melanosomes. The endolysosomal system allows reversible coloration in spiders by sustaining pigment turnover thanks to its fundamental anabolic and catabolic functions, a hypothesis first laid out for human eyes. Our findings imply that the ubiquitous endolysosomal system had been repurposed early in animal evolution to handle pigment–light interactions, providing phenotypic plasticity and cell function maintenance.