Coiled-coil peptides are frequently used to create new function upon the self-assembly of supramolecular complexes. A multitude of coil peptide sequences provides control over the specificity and stability of coiled-coil complexes. However, comparably little attention has been paid to the development of methods that allow the reversal of complex formation under non-denaturing conditions. Herein, we present a reversible two-state switching system. The process involves two peptide molecules for the formation of a size-mismatched coiled-coil duplex and a third, disruptor peptide that targets an overhanging end. A real-time fluorescence assay revealed that the proximity between two chromophores can be switched on and off, repetitively if desired. Showcasing the advantages provided by non-denaturing conditions, the method permitted control over the bivalent interactions of the tSH2 domain of Syk kinase with a phosphopeptide ligand.