Living systems create remarkable complexity from a limited repertoire of biological building blocks by controlling assembly dynamics at the molecular, cellular, and multicellular level. An open question is whether simplified synthetic cells can gain similar complex functionality by being driven away from equilibrium. Here, we describe a dynamic synthetic cell system assembled using artificial lipids that are responsive to both light and chemical stimuli. Irradiation of disordered aggregates of lipids leads to the spontaneous emergence of giant cell-like vesicles, which revert to aggregates when illumination is turned off. Under irradiation, the synthetic cell membranes can interact with chemical building blocks, remodeling their composition and forming new structures that prevent the membranes from undergoing retrograde aggregation processes. The remodeled light-responsive synthetic cells reversibly alter their shape under irradiation, transitioning from spheres to rodlike shapes, mimicking energy-dependent functions normally restricted to living materials. In the presence of noncovalently interacting multivalent polymers, light-driven shape changes can be used to trigger vesicle cross-linking, leading to the formation of functional synthetic tissues. By controlling light and chemical inputs, the stepwise, one-pot transformation of lipid aggregates to multivesicular synthetic tissues is feasible. Our results suggest a rationale for why even early protocells may have required and evolved simple mechanisms to harness environmental energy sources to coordinate hierarchical assembly processes.