Fluorescent proteins (FPs) have revolutionized biology as labels and sensors. Notably, only a few years after the cloning and engineering of GFP began, FPs successfully transitioned to synthetic materials for their characterization or for novel applications. This trend has only accelerated since then. Despite these advances, FPs face limitations in non-biological environments and lack resilience under unnatural stress conditions. To address this, we introduced a genetically encoded macro-oligomerization strategy that enhances FP protein-protein interactions through electrostatic control, applicable across various FPs. These macro-oligomers remain stable for months in organic solvents and harsh conditions, making them suitable for integration into non-aqueous polymer-based materials. Our computer-based engineering approach also produced highly supercharged FPs (+22) that retain photoluminescence and thermal stability comparable to their native counterparts, forming self-assembled FP-apoferritin co-crystals within silicone. Additionally, we demonstrated that all FP classes can emit circularly polarized light (CPL), achieving unprecedented CPL brightness among organic emitters. Our findings reveal that CPL emission in ?-barrel FPs is inherently linked to the chromophore’s polarity, degrees of freedom, and exciton coupling. Our findings suggest that CPL can be genetically controlled in the future.