Survival of the human malaria parasite Plasmodium falciparum in the circulation of the host relies on its ability to drastically alter its red blood cell (RBC) host cell. This remodelling is mediated by the export of parasite-derived proteins that interact and change the physical properties of the host cell, allowing asexual stage parasites to cytoadhere in the microvasculature and sexual stages to sequester within the bone marrow. We functionally asses the RBC membrane skeleton remodelling processes across both asexual and sexual blood stage (Gametocyte) development, by combining parasite reverse genetics with ektocytometry, spleen mimic filtration assays, super resolution microscopy and atomic force microscopy techniques. Measurements of the membrane skeleton show a stretching of the membrane skeleton network and that reorganization of the actin-spectrin membrane are associated with increases in parasite rigidity. We show that rearrangements of the RBC membrane skeleton underpin shifts in RBC deformability properties. In addition, we show that this process is differentially regulated in the asexual and sexual stages with sexual stage parasites, not expressing kahrp and knobs at the erythrocyte membrane. In addition, other exported parasite proteins known to drive rigidity changes in the asexual stage parasite are also absent from the sexual stages of development. We show that these RBC modifications of the early stage gametocyte are reversed in the late stage gametocyte with a relaxing of the membrane skeleton driving an increase in deformability. This shift in deformability coincides with the release of late stage gametocytes from the bone marrow into the the circulation allowing the parasite to survive within the host and facilitate disease transmission.