Highly conserved intraflagellar transport (IFT) protein complexes direct both the assembly of primary cilia and the trafficking of signaling molecules. IFT complexes initially accumulate at the base of the cilium, and periodically enter the cilium suggesting a yet identified mechanism that triggers ciliary entry of IFT complexes. Using AP-MS purification of interactors of the centrosomal and ciliopathy protein, CEP19, we identify CEP350, FOP and the RABL2 GTPase as proteins organizing the first known mechanism directing ciliary entry of IFT complexes. We discover that CEP19 is recruited to the ciliary base by the centriolar CEP350/FOP complex, and then specifically captures GTP-bound RABL2B, which is activated via its intrinsic nucleotide exchange. Activated RABL2B then captures and releases its single effector, the intraflagellar transport B holocomplex, from the large pool of pre-docked IFT-B complexes and thus initiates ciliary entry of IFT.