Septins are conserved cytoskeletal structures functioning in a variety of biological processes including cytokinesis and cell polarity. A wealth of information exists on the heterooligomeric architecture of septins and their subcellular localisation at distinct sites. However, the precise mechanisms of their subcellular assembly and their intracellular transport are unknown. Here, we demonstrate that endosomal transport of septins along microtubules is crucial for formation of higher-order structures in Ustilago maydis. Importantly, endosomal septin transport is interdependent providing strong evidence that septin heteromeric complexes are assembled on endosomes. Furthermore, endosomal trafficking of all four septin mRNAs is required for endosomal localisation of their translation products. Based on these results we propose that local translation promotes the assembly of newly synthesized septins in heteromeric structures on the surface of endosomes. This is important for the long-distance transport of septins and the efficient formation of the septin cytoskeleton.