Biogenesis of motile cilia in multiciliated cells (MCCs) is coupled to large-scale biosynthesis of force generating dynein motors. Shulin inhibits pre-assembled ODA (outer dynein arm) motors by packaging them into a closed conformation preventing aberrant off-target interactions with cellular microtubules in multiciliated Tetrahymena cells and co-localises with them in growing cilia. How packaged ODAs engage the Intraflagellar Transport machinery (IFT) to transit from the cytoplasm into growing cilia remains unclear. The mechanism of Shulin’s release for ODA activation inside cilia is also poorly resolved. Using proteomics, we establish links between DNAAF9 (human Shulin) and mammalian ODAs, the anterograde IFT-B complex and a ciliary small GTPase called ARL3. Based on our findings, we propose that Shulin/DNAAF9 enforces ODA inhibition to aid their unimpeded trafficking from the cytoplasm into growing multicilia via IFT and once inside the ciliary compartment, ARL3-GTP competes for a binding site to destabilise the ODA-Shulin complex thereby promoting ODA motor activation.