The Gram-negative outer membrane (OM) is densely packed with outer membrane proteins (OMPs) that are folded into β-barrel structures. OMPs form one of the major components of the host-pathogen interface. Despite their structural and functional diversity, the majority of newly synthesised OMPs are folded and integrated by the essential Barrel Assembly Machine (BAM). However, the molecular process of OMP folding by BAM has remained largely a mystery. Major questions include: (1) how are new OMPs recognised by BAM in the folding pathway? (2) what is the energy source for folding? To solve these questions, we tracked protein folding in bacterial culture and observed folding intermediates in OM native-nanodiscs by Cryo-Electron Microscopy. Our data leads to unique models of OMP biogenesis wherein the surface tension across the OM macrostructure can power OMP folding at the molecular level. This work has implications for understanding how Gram-negative pathogens build the majority of their OMP virulence factors and in the design of new antibiotics that target OMP folding at the bacterial cell surface.