Holoparasitic plants of the genus Cuscuta are unable to photosynthesize and penetrate shoots of host plants with haustoria. With a haustorium Cuscuta spp. build a connection to the host vasculature to exhaust water, solutes and carbohydrates. Such infections usually stay unrecognized by the host and lead to host plant damage. During the haustorium penetration phase, the cells of the ingrowing parasitic haustorium require nutrients, energy and sugars but do not yet possess a symplasmic connection to host plant cells. How are parasite cells supplied with nutrients and energy during the first week of the infection process? Addressing this question, we discovered and studied a set of membrane transport proteins, genes of which are sequentially expressed and that are involved in an apoplastic nutrition mechanism. Our findings demonstrate how the early parasitic prehaustorial cells are first provided with sugars from parasite’s storages and how they later switch to acquire nutrients from host cells’ apoplast as early as possible and before a connection to host vascular bundles. These findings shed light on the early nutrition strategies of Cuscuta spp. that are taking place during the days before a connection to host vasculature.