The inducible biosynthesis of chlorophylls d and f enables a subset of specialised cyanobacteria to perform oxygenic photosynthesis under far-red light—in the absence of visible wavelengths—via a process termed far-red light photoacclimation. These pigments, like the more common chlorophylls a and b, typically carry an ethyl substituent at the C8 position of the macrocycle, formed by reduction of a vinyl group by an 8-vinyl reductase enzyme. Here, we disrupted the gene encoding BciB, an 8-vinyl reductase found in the majority of cyanobacteria, in Chroococcidiopsis thermalis PCC 7203, a model organism for studying far-red light photoacclimation. Disruption of bciB results in the synthesis of 8-vinyl chlorophyll a when cells are grown in white light; upon switching to far-red light, 8-vinyl forms of chlorophylls d and f, which have not been detected in nature, are synthesised in this strain. The bciB mutant exhibits sensitivity to high irradiance under both light regimes. Pigment analysis and whole-cell absorption and fluorescence spectroscopy reveal decreased synthesis of far-red absorbing chlorophylls, reduced photosystem assembly and an impaired acclimation to far-red light, and transmission electron microscopy demonstrates altered thylakoid membrane morphology in the mutant when compared to the wild type. These results demonstrate the importance of 8-vinyl group reduction for acclimation to far-red light.