Kinesins are motor proteins found in all eukaryotic lineages that move along microtubule tracks to mediate several cellular processes such as mitosis and intracellular transport of cargo. In trypanosomatids, the kinesin protein superfamily has undergone a prominent expansion, giving these protists one of the most diverse kinesin repertoires in eukaryotes. This has led to the emergence of two trypanosomatid-restricted groups of kinesins. Here, we characterize in Trypanosoma brucei TbKifX2, a hitherto orphaned kinesin that belongs to one of these groups. TbKifX2 tightly interacts with TbPH1, a kinesin-like protein named after a pleckstrin homology (PH) domain present within its carboxy terminal tail. TbKifX2 recruits TbPH1 to the microtubule quartet (MtQ), a characteristic cytoskeletal structure that runs adjacent to the flagellar attachment zone filament from the basal body to the anterior of the cell. The proximal proteome of TbPH1 has revealed four proteins that localize to structures found adjacent to the length of the MtQ, further confirming that the likely TbKifX1/TbPH1 heterodimer binds the MtQ along its whole length. Simultaneous ablation of both TbKifX2 and TbPH1 leads to the formation of prominent extrusions from the cell posterior. Thus, we have attributed a morphogenesis role to these two trypanosomatid-restricted proteins, and the unique cytoskeletal structure represented by the MtQ. We hypothesize that the putative TbKiX2/TbPH1 heterodimer may transport a cytokinesis auxiliary factor(s) along the MtQ to or from the T. brucei posterior. The cohort of proteins found in proximity to TbPH1 may represent one of these factors directly or be involved in their trafficking during cell division in trypanosomatids.