Although facilitated cellular entry of substrates with thiol-reactive motifs has been observed for decades, this so-called thiol-mediated uptake (TMU) remains poorly understood. We have proposed a mechanism of entry involving cellular proteins that form reversible dynamic covalent bonds with thiol-reactive cascade exchangers (CAXs), which is challenging to prove because the substrate-protein bond is transient and constantly shifting. Thus, with conventional proteomics analysis of TMU, continuing exchange during processing should result in labeling of the inert binders rather than the best exchangers, that is, repressors and intracellular targets, instead of the enablers of TMU. Any static covalent bonding to a binding site will also perturb the molecular relay network of interest. The emerging photocatalytic microenvironment mapping (μMap) proteomics, however, promises to catch snapshots of off-equilibrium relay networks without disturbing their flow. Exchange partners that are temporarily within <4 nm radius of photocatalyst-CAX conjugates should be irreversibly biotinylated without systematically interfering with TMU. μMap proteomics of this elusive flow of TMU was explored for three different photocatalyst-CAX conjugates. They were measured against CAX-free photocatalyst controls and dynamic covalent TMU inhibitors. Validated by genetic knockdown, solute carriers (MFSD5, SLC29A2), flippases (ATP11C), and tetraspanins (TSPAN8) are identified as primary exchange partners. This is rewarding because their canonical functions already involve local membrane reorganization. The result is a new understanding of the nature of TMU, which will be helpful to guide future progress toward control over cell penetration for drug delivery and drug discovery. It also highlights the unique potential of photocatalytic proximity labeling proteomics to elucidate off-equilibrium molecular relay networks without disturbing their flow.