G protein-coupled receptors (GPCRs) drive intracellular signaling in response to extracellular ligands, but our understanding of how this signaling is spatiotemporally organized is limited. Here we focus on the metabotropic glutamate receptors (mGluRs), a key family of GPCRs which respond to complex patterns of neurotransmitter release to modulate synaptic transmission. To manipulate mGluRs with high spatial and temporal control to better reproduce their native, physiological activation dynamics than classical pharmacology, we developed new photopharmacological tools. Photoswitchable, orthogonal, tethered ligands (PORTLs) enable the activation of Group I (mGluR1, mGluR5) and Group II (mGluR2, mGluR3) mGluRs using targeted light application in neurons and astrocytes. This approach enabled the discovery that local activation of mGluR5 in astrocytic processes produces local oscillatory Ca2+ signaling dynamics that are distinct from the response to global drug application. In addition, we characterized a role for G protein-coupled receptor kinases (GRKs) in rapid regulation of Group I mGluR-mediated Gq-coupled receptor signaling via GRK2/3 binding to the Gq subunit directly to desensitize signaling. This form of desensitization generalizes across Gq-coupled GPCRs and may represent a widespread, underappreciated form of GPCR regulation. Together this work establishes a technical and mechanistic framework for future high resolution optical studies of mGluR signaling dynamics in physiological contexts.