The ability of Gram-negative bacteria to adapt and respond to environmental change, is essential for their survival. A key element in this colonisation is the outer membrane (OM), which is rich in integral β-barrel proteins that have roles in cell adhesion, cell signalling, the uptake of nutrients and small molecules, including antimicrobials, and can act as virulence factors. Contrary to accepted dogma, these outer membrane proteins (OMPs) form an asymmetric proteolipid membrane rather than an asymmetric lipid bilayer. The underlying molecular network of OMP-lipid-OMP interactions that span the cell surface are essential for forming a structure that couples the requisite multi-functionality of the OM to its stability and impermeability. Invagination of this rigid OM at division septa is a major undertaking for Gram-negative bacteria, requiring the Tol-Pal system and cellular energy. Tol-Pal proteins assemble into a cell envelope spanning complex that transfers energy from the proton motive force (PMF) operating at the inner membrane to drive envelope stabilising interactions at the OM. Here we present structural, biophysical, and biochemical data that resolves how OMPs form supramolecular clusters that organise the OM and how the Tol-Pal system exploits the PMF to ensure OM invagination at division sites