Cyanobacteriochromes (CBCRs) form a large, spectrally diverse family of photoreceptors (linear tetrapyrrole covalently bound via a conserved cysteine) that perceive ultraviolet to red light. The underlying mechanisms are reasonably well understood with, in certain cases, reversible formation of an adduct between a second cysteine and the chromophore accounting, in part, for their spectral diversity. These CBCRs are denoted as dual-Cys CBCRs, and most such CBCRs had been shown to reversibly absorb blue and green light. Herein, we report the structural and mechanistic characterization of a new type of dual-Cys CBCR, AM1_1186, which exhibits reversible photoconversion between a red-absorbing dark state (λmax = 641 nm) and a blue-absorbing photoproduct (λmax = 416 nm). The wavelength separation of AM1_1186 photoconversion is the largest found to date for a CBCR. In addition to one well-conserved cysteine responsible for covalent incorporation of the chromophore into the apoprotein, AM1_1186 contains a second cysteine in a unique position of its photosensory domain, which would be more properly classified as a red/green CBCR according to its sequence. Carboxyamidomethylation and mutagenesis of the cysteines revealed that the second cysteine forms an adduct with the tetrapyrrole, the phycocyanobilin, that can be reversed under blue light. The proline immediately upstream of this cysteine appears to determine the rate at which the cysteinylation following photoexcitation of the dark state chromophore can occur. We propose a possible reaction scheme and color-tuning mechanism for AM1_1186 in terms of its structure and its place in a phylogenetic tree.