The phosphoinositide 3-kinase (PI3K) pathway regulates multiple steps in glucose metabolism and also cytoskeletal functions, such as cell movement and attachment. Here, we show that PI3K directly coordinates glycolysis with cytoskeletal dynamics in an AKT-independent manner. Growth factors or insulin stimulate the PI3K-dependent activation of Rac, leading to disruption of the actin cytoskeleton, release of filamentous actin-bound aldolase A, and an increase in aldolase activity. Consistently, PI3K inhibitors, but not AKT, SGK, or mTOR inhibitors, cause a significant decrease in glycolysis at the step catalyzed by aldolase, while activating PIK3CA mutations have the opposite effect. These results point toward a master regulatory function of PI3K that integrates an epithelial cell’s metabolism and its form, shape, and function, coordinating glycolysis with the energy-intensive dynamics of actin remodeling. Display omitted •PI3K signaling positively regulates aldolase activity in epithelial cells•PI3K activation mobilizes aldolase from F-actin, increasing flux through glycolysis•PI3K-to-aldolase signaling occurs through Rac and not through AKT•PI3K coordinates cytoskeletal dynamics and glycolysis in vitro and in vivo Phosphoinositide 3-kinase directly coordinates glycolysis by activating Rac, which remodels the actin cytoskeleton to free actin-bound aldolase.