Bacterial microcompartments (BMC) are protein organelles with diverse metabolic capabilities. Their functional diversity is determined by an enzymatic core that is sequestered within a structurally conserved protein shell architecture. Segregation of protein cargo into the BMC is enabled by encapsulation peptides (EPs), which are short helical domains fused to core proteins through a disordered linker. Here, we investigate how EPs drive multicomponent cargo assembly into biomolecular condensates.In vitroexperiments supported by molecular dynamics simulations demonstrate the importance of both conserved hydrophobic packing and electrostatic interactions in stabilizing trimeric EP bundles. Topological rearrangements of EP domains can drive programmable liquid-or gel-like partitioningin vitroandin vivo. This partitioning is found to be EP-specific, modular and can co-assemble at least three fluorescent reporters. In summary, we describe the molecular features necessary to drive biomolecular condensation using a widespread peptide tag. This work can serve as a blueprint for implementing EP biotechnology across diverse applications.