Light is essential for plant organogenesis and development. Light-regulated shoot morphogenesis has been extensively studied; however, the mechanisms by which plant roots perceive and respond to aboveground light are largely unknown, particularly because the roots of most terrestrial plants are usually located underground in darkness. To mimic natural root growth conditions, we developed a root-covered system (RCS) in which the shoots were illuminated and the plant roots could be either exposed to light or cultivated in darkness. Using the RCS, we observed that root growth of wild-type plants was significantly promoted when the roots were in darkness, whereas it was inhibited by direct light exposure. This growth change seems to be regulated by ELONGATED HYPOCOTYL 5 (HY5), a master regulator of photomorphogenesis. Light was found to regulate expression in the roots, while a HY5 deficiency partially abolished the inhibition of growth in roots directly exposed to light, suggesting that expression is induced by direct light exposure and inhibits root growth. However, no differences in expression were observed between illuminated and dark-grown roots, indicating that HY5 may be regulated by COP1-mediated proteasome degradation. We confirmed the crucial role of HY5 in regulating root development in response to light under soil-grown conditions. A transcriptomic analysis revealed that light controls the expression of numerous genes involved in phytohormone signaling, stress adaptation, and metabolic processes in a HY5-dependent manner. In combination with the results of the flavonol quantification and exogenous quercetin application, these findings suggested that HY5 regulates the root response to light through a complex network that integrates flavonol biosynthesis and reactive oxygen species signaling. Collectively, our results indicate that HY5 is a master regulator of root photomorphogenesis.