We found a new, versatile, dynamic covalent bond that exists only out of equilibrium at the expense of chemical energy. The tyrosine ester-based dynamic covalent bond creates a dynamic combinatorial library by expanding a chemical reaction cycle based on EDC and aspartic acid-derived peptides with an esterification pathway. We found the new bond gives rise to a dynamic mixture of cyclic and linear tyrosine esters that form intraand intermolecularly. The kinetics of the chemical reactions are quantitatively understood, allowing us to tune the product distribution through molecular design. Moreover, we showed that, through molecular design, the library could be linked to simple or complex coacervation. We envision the resulting coacervates or coacervate core micelles with lifetimes of multiple hours could be attractive for future applications, e.g., for controlled release systems for DNA or RNA. They are also valuable models for membraneless organelles, which are also coacervate-based droplets regulated through chemical reaction cycles. Finally, we envisage these droplets as a powerful protocell model or a compartment in life's de novo synthesis.