Carotenoids are plastidial isoprenoids essential for plant life. In Arabidopsis thaliana carotenoid biosynthesis is strongly upregulated when seedlings that germinate in the dark (etiolated) emerge from the soil and light derepresses photomorphogenesis, causing etioplasts to become chloroplasts. We found that carotenoid biosynthesis is also induced when deetiolation is derepressed in the absence of actual light, eventually resulting in improved greening (chlorophyll accumulation) upon illumination. The increased production of carotenoids in the dark correlates with an upregulated activity of phytoene synthase (PSY; the first committed enzyme of carotenogenesis) and the induction of PSY gene expression in cotyledons (where carotenoids accumulate in dark-grown seedlings). The metabolic precursors for carotenoid synthesis under these conditions are mostly supplied by the plastidial methylerythritol 4-phosphate (MEP) pathway. Accumulation of flux-controlling MEP pathway enzymes, such as deoxyxylulose 5-phosphate synthase (DXS), is post-transcriptionally increased when deetiolation is derepressed in the dark. Unlike the situation observed in light-grown plants, however, the sole overexpression of DXS in dark-grown seedlings does not increase carotenoid accumulation. By contrast, induced expression of a PSY-encoding transgene results in increased carotenoid levels and a concomitant post-transcriptional accumulation of DXS. These data provide evidence for a feedback mechanism by which PSY controls metabolic flux to the carotenoid pathway in plants.