Phytochromes are red/far-red-light detecting photoreceptors that regulate plant growth and development. They photo-interconvert between an inactive Pr (red-light absorbing) and a physiologically active Pfr (far-red-light absorbing) form, acting as light-controlled molecular switches. Although the two major plant phytochromes A (phyA) and B (phyB) share similar absorption properties, they exhibit dramatic differences in their action spectra. Since both phytochromes antagonistically regulate seedling development under vegetative shade, it is essential for plants to clearly distinguish between phyA and phyB action. This discrimination is not comprehensible solely by the molecular properties of the phytochromes, but is evidently due to the dynamics of the phytochrome system. Using an integrated experimental and mathematical modelling approach we show that phytochrome dimerization is an essential element for phyB function. Our findings reveal that light-independent Pfr to Pr relaxation (dark reversion) and association/dissociation to nuclear bodies (NBs) severely depend on the conformational state of the phyB dimer. We conclude that only Pfr-Pfr homodimers of phyB can be responsible for triggering physiological responses, leading to a suppression of phyB function in the far-red range of the light spectrum.