Cyanobacteria use soluble antenna megacomplexes, phycobilisomes (PBS), to maximize light-harvesting efficiency and small photoswitchable orange carotenoid proteins (OCPs) to down-regulate PBS in high light. Among known PBS morphologies, the one from the basal cyanobacterial genus Gloeobacter still lacks detailed structural characterization. Here, we present the cryo-EM structure of the G. violaceus PBS, a >10-MDa complex with a unique architecture consisting in 516 polypeptide chains totaling nearly 90,000 residues and harboring over 860 bilin chromophores. This unique PBS features diverging, conformationally mobile bundles of rods composed of stacked phycoerythrin and phycocyanin hexamers, stemming from a pentacylindrical allophycocyanin core belted by auxiliary phycocyanin hexamers. We show how two Gloeobacter-specific multidomain linker proteins, Glr1262 and Glr2806, maintain this bundle-shaped architecture and reveal its differential regulation via non-photochemical quenching by two OCP types of G. violaceus that recognize separate binding sites within the allophycocyanin core, including lateral cylinders absent in tricylindrical cores. Our findings provide the high-resolution structural insight into Gloeobacter PBS and its regulation, revealing divergent adaptations in early-branching cyanobacteria. The structure advances understanding of PBS diversity and evolution, offering a framework for bioengineering light-harvesting systems in synthetic biology and biotechnological applications.