The transmission of malaria parasites relies on the formation of a specialized blood form of the parasite called the gametocyte. The gametocyte undergoes remarkable changes in its shape, physiology and biophysical properties as it prepares for transmission to mosquitoes. The unique crescent shape of Plasmodium falciparum gametocytes, is driven by the assembly of a network of microtubules that are supported by an underlying membrane structure called the inner membrane complex (IMC). Using super-resolution optical microscopy and electron microscopy we define the ultrastructure of the IMC at different stages of gametocyte development. We characterize two new proteins of the gametocyte IMC, called PhIL1 and PIP1. Genetic disruption of PhIL1 or PIP1 ablates elongation and prevents formation to transmission-ready mature gametocytes. The maturation defect is accompanied by a failure to form an enveloping IMC and a marked swelling of the digestive vacuole, suggesting PhIL1 and PIP1 are required for correct membrane trafficking. Using GFP tagged PhIL1 and PIP1 in an immunoprecipitation and mass spectrometry based approach we have characterized the interacting partners of these proteins and identified new protein components of the IMC in gametocytes.