Aerial roots of epiphytic orchids possess a velamen structure that is assumed to assist water uptake and reduce water loss. However, there is still debate over how this dual function is achieved. The discovery of a water-repelling layer that covers the velamen may provide answers. To determine what role this layer plays in velamen function, we examined the structure, chemical composition, gene expression, wettability and water loss prevention of epiphytic orchid roots. Results of our analyses indicate this water-repelling layer is similar to the plant cuticle. Therefore, we have named it the “cuticle-like layer”. Further analysis of epiphytic roots showed that when the velamen was in contact with bark, genes related to cuticle biosynthesis were down-regulated and root hairs developed. Furthermore, in root tissues close to bark, aquaporin gene expression responded positively to water-supply. The functional paradox of the velamen can be explained by a “functional zoning” hypothesis: epiphytic orchid roots are partitioned into spatially-separated regions that prevent water loss and increase water absorption. At different regions of the velamen, water loss is prevented by the development of a cuticle-like layer, and water absorption is increased by the development of root hairs.