The particular virulence of the most deadly of the malaria parasites, Plasmodium falciparum, is associated with binding of infected red blood cells (RBCs) to sites in the brain and the placenta. Adhesion is mediated by a Velcro-like protein, called P. falciparum erythrocyte membrane protein-1 (PfEMP1), presented at the RBC surface. Despite its importance, the mode of trafficking of PfEMP1 and its insertion into the RBC membrane is poorly studied. We have used super-resolution microscopy, electron tomography and molecular methods to probe the organisation of the membrane network that the parasite establishes in its host cell to traffic PfEMP1 to the RBC surface via. We have examined exomembrane sculpting proteins, such as the ring-exported protein-1 (REX1), and followed the trafficking pathway for the major virulence protein, P. falciparum erythrocyte-binding protein-1 (PfEMP1). We have defined the REX1 domains responsible for Maurer's cleft sculpting. We have examined the trafficking of a GFP chimera of PfEMP1 expressed in transfected parasites and show that it is trafficked via a specialised compartment at the parasite surface, before transfer to the surface via Maurer's clefts and electron-dense vesicles. We show that parasitophorous vacuole-located PfEMP1B interacts directly with components of the Plasmodium Translocon of EXported (PTEX) as well as a novel protein complex we refer to as the Exported Protein-Interacting Complex (EPIC). We define the EPIC interactome and use an inducible knockdown system to show that depletion of one of the components, the parasitophorous vacuole protein-1 (PV1), results in attenuation of the cytoadhesion of P. falciparum-infected RBCs to endothelial cell ligands.