Caveolae are spherical nanodomains of the plasma membrane in metazoans, generated by cooperative assembly of two protein families called Caveolins and Cavins. Caveolins are integral membrane proteins, while Cavins are cytosolic peripheral membrane proteins essential for caveola formation in tissues including adipocytes, muscle fibres and endothelium. Cavins possess distinctive primary and secondary structures, with an alternating distribution of intrinsically disordered regions (DRs) and a-helical regions (HRs) rich in negatively and positively charged residues respectively. While the HR domains are required for coiled-coil assembly and binding to the phospholipid membrane, the role of the extended DR domains is unknown. Here we show that the three intrinsically disordered DR domains of Cavin1 are essential for caveola formation, with mutations or deletions leading to disruption of caveolar protein coat dynamics and perturbed interactions with Caveolin-1 (CAV1) at the plasma membrane. These defects also correlate with an inability of recombinant forms of Cavin1 to reshape synthetic membranes in vitro. Electrostatic interactions between DR and HR regions can promote liquid-liquid phase separation (LLPS) behaviour of Cavin1 in vitro, drive assembly of Cavin1 polymers in solution, and regulate the recruitment of Cavin1 to caveolae in cells. We propose a model for caveola assembly whereby ‘fuzzy’ electrostatic interactions between Cavin1 proteins, combined with CAV1 and membrane lipid interactions are required to generate a metastable caveola coat structure.