While some self-sustaining compartments have been described with exciting behavior like growth and even division, the number of examples that form vesicle-based compartments remains limited. Moreover, examples that produce self-sustaining compartments based on prebiotically plausible chemistry are scarce. In this work, we developed a self-sustaining chemical system that produces non-equilibrium, transient vesicles based on simple, prebiotically plausible building blocks (Scheme 1). Specifically, we used fatty acids combined with alkyl phosphates as building blocks. When supplied with carbodiimides or prebiotically plausible activating agents, a reaction cycle operates that produces acyl phosphates as an activated product. That product is labile and hydrolyzed to its precursor. However, in its activated state, despite its short lifetime, it can assemble to form dynamic vesicles. These vesicles emerge in response to activating agents.