Plasmodium falciparum is the most virulent human malaria parasite, accounting for the overwhelming majority of malaria-related deaths each year. P. falciparum parasites invade red blood cells (RBCs) and extensively modify the structure and morphology of their host cell by generating and exporting a range of parasite proteins. One key parasite protein, P. falciparum Erythrocyte Membrane Protein-1 (PfEMP1), is trafficked to the surface of infected RBCs where it mediates adhesion to the vascular endothelium of the human host. This study has investigated multiple facets of the complex protein trafficking pathway undertaken by PfEMP1 prior to presentation on the surface of infected RBCs. We have examined the trafficking of PfEMP1-GFP chimera in very early stage parasites to show PfEMP1 molecules accumulate in novel discrete foci at the parasite surface prior to further export to small parasite-generated exomembranous structures in the cytoplasm of the host RBC, known as Maurer’s clefts. In an effort to further elucidate the role of the parasite exomembrane system, we have used tightly synchronised parasite-infected RBCs to investigate the development and organisation of Maurer’s clefts and small membranous tether structures, or simply 'tethers', over the first 24 hours of the parasite lifecycle. Here we demonstrate that tethers are generated much earlier than previously thought and appear to latch onto the Maurer’s cleft structures. While initially mobile and freely moving throughout the host RBC cytoplasm, these Maurer’s cleft-tether complexes eventually dock onto the host RBC membrane by 20-24 hours post-invasion. Finally, we have explored a potential role of host actin remodelling in the final-step trafficking of PfEMP1 to the RBC surface by showing reduction in PfEMP1 surface presentation following treatment with drugs affecting actin polymerisation and stability.