The authors present a genetically encoded, light-switchable protein-protein interaction system based on the phytochrome signaling network of *Arabidopsis thaliana*. This system, optimized for reversible and rapid translocation of target proteins to the plasma membrane, allows for precise and controlled manipulation of cellular processes. The interaction between phytochrome B (PhyB) and Phytochrome Interaction Factor 3 (PIF3) is used to achieve this control, with light-gated translocation occurring at micrometer spatial resolution and second time resolution. The system is demonstrated to be effective in mammalian cells, enabling the precise reshaping and direction of cell morphology by controlling the activity of rho-family GTPases, which regulate the actin cytoskeleton. The authors show that this light-gated protein-protein interaction can be used to design diverse light-programmable reagents, potentially revolutionizing perturbative and quantitative experiments in cell biology. The high spatial and temporal resolution of the light control allows for the creation of complex spatial or temporal patterns to drive cellular processes, offering a novel analytical tool for studying cell biology.The authors present a genetically encoded, light-switchable protein-protein interaction system based on the phytochrome signaling network of *Arabidopsis thaliana*. This system, optimized for reversible and rapid translocation of target proteins to the plasma membrane, allows for precise and controlled manipulation of cellular processes. The interaction between phytochrome B (PhyB) and Phytochrome Interaction Factor 3 (PIF3) is used to achieve this control, with light-gated translocation occurring at micrometer spatial resolution and second time resolution. The system is demonstrated to be effective in mammalian cells, enabling the precise reshaping and direction of cell morphology by controlling the activity of rho-family GTPases, which regulate the actin cytoskeleton. The authors show that this light-gated protein-protein interaction can be used to design diverse light-programmable reagents, potentially revolutionizing perturbative and quantitative experiments in cell biology. The high spatial and temporal resolution of the light control allows for the creation of complex spatial or temporal patterns to drive cellular processes, offering a novel analytical tool for studying cell biology.