SummaryXanthophyll cycles are broadly important in photoprotection, and the reversible de‐epoxidation of xanthophylls typically occurs in excess light conditions. However, as presented in this review, compiling evidence in a wide range of photosynthetic eukaryotes shows that xanthophyll de‐epoxidation also occurs under diverse abiotic stress conditions in darkness. Light‐driven photochemistry usually leads to the pH changes that activate de‐epoxidases (e.g. violaxanthin de‐epoxidase), but in darkness alternative electron transport pathways and luminal domains enriched in monogalactosyl diacyl glycerol (which enhance de‐epoxidase activity) likely enable de‐epoxidation. Another ‘dark side’ to sustaining xanthophyll de‐epoxidation is inactivation and/or degradation of epoxidases (e.g. zeaxanthin epoxidase). There are obvious benefits of such activity regarding stress tolerance, and indeed this phenomenon has only been reported in stressful conditions. However, more research is required to unravel the mechanisms and understand the physiological roles of dark‐induced formation of zeaxanthin. Notably, the de‐epoxidation of violaxanthin to antheraxanthin and zeaxanthin in darkness is still a frequently ignored process, perhaps because it questions a previous paradigm. With that in mind, this review seeks to shed some light on the dark side of xanthophyll de‐epoxidation, and point out areas for future work.