The plasma membranes of many cell types are decorated by ~60 nm membrane invaginations called caveolae – “little-caves”. Caveolae are especially abundant in cells of muscle, heart, endothelial and adipose tissues. Their formation requires coordinated association of peripheral membrane proteins called cavins and membrane-integral proteins called caveolins. Functionally, caveolae are important in endocytosis, lipid homeostasis and cell signalling, and also play an important role in maintaining membrane integrity during mechanical stress. Mutation and dysregulation of these proteins result in systemic pathologies with severe symptoms in heart and skeletal muscles, lipodystrophy and general metabolic disorders. Despite their importance, there is currently no high-resolution structural information addressing the mechanisms that underpin caveola formation. Here we describe the first structure determination of a protein domain required for cavin assembly and membrane recruitment. Sequence analysis identified two putative helical regions (HR1 and HR2) flanked by three disordered regions (DR1 through DR3) in all cavins. Further truncation studies identified the HR1 domain as the minimal fragment controlling homo- and hetero-association of cavins. Crystallographic structure determination revealed the HR1 domain to be a trimeric coiled-coil, thereby identifying trimerisation as the first step in hierarchical assembly of cavin complexes. The HR2 domain was found to promote a second stage of higher-order oligomerisation, and along with HR1 provided a second binding site negatively-charged lipids required for membrane recruitment. Electron microscopy of the full-length cavin proteins revealed an elongated rod-like structure, which we suggest is partly composed of these rigid coiled-coil domains, and represents the fundamental structural unit of the striated coats that characterise caveolae in vivo. Overall this work presents an important step towards a full molecular understanding of caveola structure.