Bardet-Biedl syndrome (BBS) is a ciliopathy caused by defects in the assembly or distribution of the BBSome, a conserved protein complex. The BBSome cycles via intraflagellar transport (IFT) through cilia to transport signaling proteins. How the BBSome is recruited to the basal body for binding to IFT trains for ciliary entry remains unknown. Here, we show that the Rab-like 5 GTPase IFT22 regulates basal body targeting of the BBSome in Chlamydomonas reinhardtii. Our functional, biochemical and single particle in vivo imaging assays show that IFT22 is an active GTPase with low intrinsic GTPase activity. IFT22 is part of the IFT-B1 subcomplex but is not required for ciliary assembly. Independent of its association to IFT-B1, IFT22 binds and stabilizes the Arf-like 6 GTPase BBS3, a BBS protein that is not part of the BBSome. IFT22/BBS3 associates with the BBSome through an interaction between BBS3 and the BBSome. When both IFT22 and BBS3 are in their guanosine triphosphate (GTP)-bound states they recruit the BBSome to the basal body for coupling with the IFT-B1 subcomplex. The GTP-bound BBS3 likely remains to be associated with the BBSome upon ciliary entry. In contrast, IFT22 is not required for the transport of BBSomes in cilia, indicating that the BBSome is transferred from IFT22 to the IFT trains at the ciliary base. In summary, our data propose that nucleotide-dependent recruitment of the BBSome to the basal body by IFT22 regulates BBSome entry into cilia. Significance Bardet-Biedl syndrome (BBS) is a rare human ciliopathy associated with blindness, obesity, and kidney anomalies. It is caused by defects in the assembly or transport of the BBSome, a conserved octamer of BBS proteins, which assists intraflagellar transport (IFT) with the removal of signaling proteins from cilia. Here, we show that the GTPase component of IFT-B1, IFT22, autonomous of IFT-B1 association, binds and stabilizes BBS3 in the cell body. When both are in their GTP-bound state, IFT22 and BBS3 recruit the BBSome to the basal body for loading onto the IFT machinery for ciliary entry. IFT22 recruits the BBSome to the basal body through BBS3 in a nucleotide-dependent manner providing a regulatory mechanism for BBSome entry into the cilium.