Flagella and cilia are elaborate cytoskeletal structures conserved from protists to mammals, where they fulfil functions related to motility or sensitivity. We demonstrate a novel role for the flagellum in the control of cell morphogenesis and division of Trypanosoma brucei. To investigate flagellum functions, its formation was perturbed by inducible RNA interference silencing of components required for intraflagellar transport (IFT), a dynamic process necessary for flagellum assembly. First, we show that down-regulation of IFT leads to assembly of a shorter flagellum. Strikingly, cells with a shorter flagellum are smaller, with a direct correlation between flagellum length and cell size. Detailed morphogenetic analysis reveals that the tip of the new flagellum defines the point where cytokinesis is initiated. Furthermore, when new flagellum formation is completely blocked, non-flagellated cells are very short, lose their normal shape and polarity and fail to undergo cytokinesis. We show that flagellum elongation controls formation of cytoskeletal structures present in the cell body that act as molecular organisers of the cell.