<p>Membraneless organelles seen in extant biology leverage biochemical energy sources to realize intracellular non-equilibrium microcompartments. Constructing their synthetic mimics from small molecules can contribute towards our understanding of active phase separation and their role in the chemical emergence of compartments. Herein, we develop a model of synthetic membraneless organelles as non-equilibrium droplet phase and are accessed via homotypic interactions between small activated molecule and short peptide. The constituent short peptide’s residues mimic hydrolase-like activity via covalent catalysis which leads to vacuolization and subsequent generation of the dissolved equilibrium phase as a function of time. Despite the short tetrameric sequence, the peptide residues help in demixing (phase separation) as well as catalysis which is critical for achieving such non-equilibrium behaviour. Importantly, the low molecular weight active coacervates behave like chiral microenvironment, which further promotes kinetic resolution in chemical transformations, thus mirroring the dynamic and functional attributes associated with complex membraneless organelles.</p>