Spatiotemporal organization of distinct biological processes in cytomimetic compartments is a crucial step towards engineering functional artificial cells. Mimicking controlled bi‐directional molecular communication inside artificial cells remains a considerable challenge. Here we present photoswitchable molecular transport between programmable membraneless organelle‐like DNA coacervates in a synthetic microcompartment. We use droplet microfluidics to fabricate membraneless non‐fusing DNA coacervates by liquid‐liquid phase separation in a water‐in‐oil droplet, and employ the interior DNA coacervates as artificial organelles to imitate intracellular communication via photo‐regulated uni‐ and bi‐directional transfer of biomolecules. Our results highlight a promising new route to assembly of multicompartment artificial cells with functional networks.