Protein-protein interactions (PPIs) mediate many fundamental cellular processes and their control through optically or chemically responsive protein domains has had a profound impact on basic research and some clinical applications. Most available chemogenetic tools induce the association, i.e., dimerization or oligomerisation, of target proteins, and the few available dissociation approaches either break large oligomeric protein clusters or heteromeric complexes. Here, we have exploited the controlled dissociation of a dimeric oxidoreductase from mycobacteria (MSMEG_2027) by its native cofactor, F420, as a bioorthogonal monomerization switch in mammalian cells. We found that in the absence of F420, MSMEG_2027 forms a tight domain-swapped dimer that occludes the cofactor binding site and undergoes substantial remodelling of the N-terminal helix upon cofactor binding and associated dissolution of the dimer. We then show that MSMEG_2027 can be expressed as fusion proteins in human cells and apply it as a tool to inhibit MAPK/ERK cell signalling from a dimeric chimeric fibroblast growth factor receptor 1 (FGFR1) tyrosine kinase. This F420-dependent chemogenetic de-dimerization tool (F420-CDD) is stoichiometric, based a single domain and presents a novel molecular mechanism complementing existing methods to investigate the functionality of protein complexes in situ.