Protein function is closely tied to its localization and interactions, which can be mapped using proximity labeling (PL). Traditional PL methods, such as peroxidases and biotin ligases, suffer from toxicity or high background. While visible light-triggered photocatalytic labeling offers great potential, it is limited by light-induced background and restricted in vivo applications. Here, we present BRET-ID, an in vivo-compatible PL technology for precise mapping of membraneless organelles and transient protein-protein interactions with sub-minute temporal resolution. BRET-ID combines a genet-ically encoded photocatalyst and NanoLuc luciferase, locally generating blue light to activate the photocatalyst via biolu-minescence resonance energy transfer (BRET). This activation produces singlet oxygen, which oxidizes nearby proteins for analysis with a streamlined chemoproteomic workflow. BRET-ID enables precise mapping of ER membrane proteins without the need for spatial reference-based filtering. Leveraging its high temporal resolution, BRET-ID provides 1-minute snapshots of dynamic GPCR interactions during ligand-induced endocytosis. Additionally, BRET-ID identifies G3BP1-interacting proteins in arsenite-stressed cells and tumor xenografts, uncovering novel stress granule components, including the mTORC2 subunit RICTOR. BRET-ID serves as a powerful genetically encoded tool for studying protein local-ization and molecular interactions in living organisms.