Some plants tolerate tissue dehydration. Dehydration conditions suppress photosynthesis, exacerbating photooxidative stress. In this study, fern samples were collected from the field, desiccated in darkness, and subsequently re-watered. During dark dehydration, zeaxanthin (Z) was formed and maximal photochemical efficiency of PS II was strongly reduced. Rehydration in the dark reversed these effects. Violaxanthin de-epoxidase was responsible for the dark formation of Z as illustrated by its complete inhibition by DTT. Nonetheless, its activity was not affected by nigericin, indicating that Z formation in the dark could be a process independent of the transmembrane pH-gradient into the thylakoids. Synthesis de novo of Z was rejected after blocking carotenogenesis with norfluorazon. Dark formation of Z was also observed in dehydrating leaves of desiccation-intolerant plants, which seems to indicate that this is a phenomenon scattered among different taxa within the plant kingdom. Plants may trigger this mechanism during dehydration, for chlorophyll protection during desiccation, and for faster acclimation when rehydrating conditions return. Violaxanthin de-epoxidation to form Z is typically a light-dependent process, but the formation induced solely by dehydration might represent an anticipatory mechanism for preventing early morning photodamage in desiccation-tolerant plants such as the fern Ceterach officinarum.