Significance At the plasma membrane an array of more than 800 G protein-coupled receptors (GPCRs) receive, convert, amplify, and transmit incoming signals. Activated GPCRs team-up with intracellular scaffolding proteins to compartmentalize signal transmission. Scaffolds, such as β-arrestin and A-kinase anchoring proteins (AKAPs), function as a physical nexus between receptors and molecular switches. Typically, these receptor-bound AKAPs recruit protein kinase A (PKA) to assemble dedicated polyvalent signaling complexes that are spatially and temporally confined. Here, we report that the orphan GPCR, Gpr161, is a PKA substrate and also has an AKAP motif embedded in its C-terminal tail. Our results suggest that Gpr161, by directly recruiting type I PKA holoenzymes to the receptor, creates a cAMP-sensing signalosome. Furthermore, we propose that Gpr161 plays a role in recruiting isoform-specific PKA complexes to primary cilia.