A genetically-encoded photoactivatable Rac (PA-Rac1) was developed to control cell motility in living cells. PA-Rac1 is a modified form of Rac1, a GTPase involved in actin cytoskeletal dynamics, which can be activated by light. The LOV domain from phototropin was fused to Rac1, allowing for reversible activation using 458 or 473 nm light. This activation leads to precise control of cell protrusions and ruffling, enabling localized Rac activation or inactivation to control cell movement direction. Myosin was involved in Rac control of directionality, while PAK was required for Rac-induced protrusion. PA-Rac1 was used to study Rac regulation of RhoA in cell motility, revealing that Rac inhibits RhoA in living cells, with inhibition modulated at protrusions and ruffles. Structural studies showed that the LOV domain occludes effector binding in the dark state, and that a mutation (F56W) in Cdc42 improved LOV inhibition of Cdc42 binding to PAK. These findings demonstrate that PA-Rac1 can serve as a blueprint for engineering other caged GTPases. PA-Rac1 enables precise spatial and temporal control of Rac activity in live cells, with reversible activation at 458 or 473 nm. Localized Rac activation or deactivation was sufficient to generate polarized cell movement. Rac could be activated without cellular compensation, enabling the study of myosin and PAK in Rac-mediated motility. Spatially-regulated Rac inhibition of Rho was demonstrated in living cells. Structural studies indicate that a non-evolved interaction at the Rac-LOV interface can be engineered to cage other GTPases. This study, along with other recent work, shows that coupling genetically encoded light-modulated domains to other proteins provides a versatile new route to control protein activities in living cells.A genetically-encoded photoactivatable Rac (PA-Rac1) was developed to control cell motility in living cells. PA-Rac1 is a modified form of Rac1, a GTPase involved in actin cytoskeletal dynamics, which can be activated by light. The LOV domain from phototropin was fused to Rac1, allowing for reversible activation using 458 or 473 nm light. This activation leads to precise control of cell protrusions and ruffling, enabling localized Rac activation or inactivation to control cell movement direction. Myosin was involved in Rac control of directionality, while PAK was required for Rac-induced protrusion. PA-Rac1 was used to study Rac regulation of RhoA in cell motility, revealing that Rac inhibits RhoA in living cells, with inhibition modulated at protrusions and ruffles. Structural studies showed that the LOV domain occludes effector binding in the dark state, and that a mutation (F56W) in Cdc42 improved LOV inhibition of Cdc42 binding to PAK. These findings demonstrate that PA-Rac1 can serve as a blueprint for engineering other caged GTPases. PA-Rac1 enables precise spatial and temporal control of Rac activity in live cells, with reversible activation at 458 or 473 nm. Localized Rac activation or deactivation was sufficient to generate polarized cell movement. Rac could be activated without cellular compensation, enabling the study of myosin and PAK in Rac-mediated motility. Spatially-regulated Rac inhibition of Rho was demonstrated in living cells. Structural studies indicate that a non-evolved interaction at the Rac-LOV interface can be engineered to cage other GTPases. This study, along with other recent work, shows that coupling genetically encoded light-modulated domains to other proteins provides a versatile new route to control protein activities in living cells.