Primary cilia exhibit a distinct complement of proteins, including G-protein-coupled receptors (GPCRs) that mediate sensory and developmental signals. The localization of GPCRs to the ciliary membrane involves ciliary localization sequences (CLSs), but it is not known how CLSs might relate to cilium type. Here, we studied the localization of two RHO-like GPCRs, SSTR3 and RHO, in three types of cilia: from IMCD3 cells, hTERT-RPE1 cells (possessing pocket cilia), and rod photoreceptors (whose cilia grow into elaborate phototransductive outer segments). SSTR3 was localized specifically to all three types of cilia, whereas RHO showed more selectivity for the photoreceptor cilium. Focusing on C-terminal CLSs, we characterized a novel CLS in the SSTR3 C-terminus, which was required for the robust ciliary localization of SSTR3. Replacing the C-terminus of RHO with this SSTR3 CLS enhanced ciliary localization, compared with full-length RHO, in IMCD3 and hTERT-RPE1 cells. Addition of the SSTR3 CLS to the single tra...