Protein misfolding and aberrant aggregation are fundamental to neurodegenerative diseases, but studying these dynamic, heterogeneous complexes within their native cellular environment remains a major challenge. We present an integrated chemical proteomics platform that enables concurrent in situ imaging, compositional profiling, and interactome mapping of the aggregated proteome in live cells. The platform combines a novel aggregate-targeting photosensitizer probe (D6) for photocatalytic proximity labeling with a biocompatible, mass-spectrometry-cleavable crosslinker, trehalose disuccinimidyl ester (TDS). This allows for the covalent capture of transient protein conformations and interactions within aggregates prior to their isolation and analysis. Applying this method to a cellular model of proteostasis stress, we identified 1,165 enriched aggregate constituents and mapped 739 protein-protein interactions (67.8% novel), revealing a densely interconnected network centered on the chaperone HSPA1B (HSP70). Functional validation demonstrated that pharmacological activation of HSP70, the central hub of this network, directly promotes the disassembly and clearance of mutant huntingtin aggregates. Our work provides a comprehensive spatial and functional atlas of the aggregated proteome and establishes a generalizable platform for uncovering the mechanisms and therapeutic targets of protein conformational diseases.