SignificanceThe motile flagellum/cilium is found across eukaryotic life, and it performs critical functions in many organisms including humans. A fundamental requirement for a motile flagellum is that it must undergo the appropriate waveform for its specific function. Much is known about the generation of asymmetry in flagellum movement; however, it is unknown how a motile flagellum specifies where waves should start and whether waves should go from base to tip, or from tip to base. We show here in two flagellum model organisms (the human parasitesTrypanosoma bruceiandLeishmania mexicana) that differences in the outer dynein arms between the distal and proximal regions of the flagellum determine wave propagation direction and are generated and maintained by the flagellum growth machinery.