Resistance to the frontline antimalarial artemisinin is mediated by mutations in the Kelch13 (K13) gene in Plasmodium falciparum. The function of K13 is unknown. Using super-resolution microscopy we showed that K13 localises to a ring at the parasite periphery and under time lapse microscopy these rings co-localise with foci of host cytoplasm as they are taken up by the parasite. We localised K13 by electron microscopy to an electron dense collar surrounding the neck of the cytostome - a double membraned invagination that allows the parasite to engulf large packages of host haemoglobin. This is the first molecular marker defined for this structure. We used a combination of 3D electron microscopic techniques (electron tomography and serial-block-face-scanning electron microscopy) to characterise Plasmodium parasites with aberrant K13. Inducible mis-localisation of K13 resulted in parasites that lack the electron dense cytostomal collar, and the parasite's tightly-constricted cytostomal neck is also lost, leading to aberrant cytostomal structures. Our data indicate that K13 is required for normal formation or stabilisation of the cytostome, and is likely a major component of the electron dense cytostomal ring itself. We show that these K13 mutant parasites have reduced uptake of haemoglobin, and consequently produce less of the haemoglobin breakdown products haem and haemozoin. Haem is required to activate artemisinin into its proteotoxic form, so a reduction in this process likely explains reduced artemisinin sensitivity. We hypothesise that K13 is required for formation of the normal cytostome used for feeding by intracellular Plasmodium, and that mutant K13 results in parasites with less efficient feeding, decreased activation of artemisinin, and ultimately, drug resistance. These data also suggest that artemisinin resistance is inextricably linked to less efficient feeding by the parasite, and suggest that further resistance through this mechanism could only come at the cost of substantially reduced parasite fitness,