Family 3 G‐protein‐coupled receptors (GPCRs) consist of the extracellular calcium‐sensing receptor (CaR), metabotropic glutamate receptors (mGluR1‐8), γ‐aminobutyric acid receptor (GABABR), taste receptors (TIR1‐3), pheromone receptors (V2Rs) and orphan receptors. These are characterized by a large amino‐terminal extracellular ligand binding domain (ECD) that is responsible for signaling and activation involving the seven‐transmembrane helical domains (7TMD). The solved crystal structure for the closed conformation of mGluR1 indicates the carboxy‐terminal portions of the monomeric units are drawn together but the signaling mechanism remains unsolved. A specific 14‐amino acid linker segment of the mGluR1 connecting the ECD to the 7TMD, present in all Family 3 GPCRs except GABABR, was critical for signaling and is consistent with the peptide‐linker model of receptor activation. To determine the relevance of this conserved motif in other Family 3 GPCRs, we altered the length and composition of the mGluR1 linker via insertion, deletion, and site‐directed mutagenesis. Phosphoinositol hydrolysis assays, ligand binding assays and calcium imaging analyses of chimeric receptors suggest that the mGluR1 linker is critical for signaling from the ECD to the 7TMD and is consistent with our finding for the CaR, supporting the peptide‐linker activation model for receptors containing this conserved motif. Work supported by the Intramural Research program of the NIDCD, National Institutes of Health.