Bacterial aggregation is a phenotype associated with disease pathogenesis. Aggregate formation enhances biofilm development, host colonization, and resistance to antibiotics and host defenses. Antigen 43 (Ag43) is a surface-located autotransporter produced by pathogenic Escherichia coli that mediates cell aggregation in biofilms. Here, two Ag43 passenger domains from neighboring bacterial cells fold into elongated β-helices and associate in a head-to-tail manner while being anchored to the cell surface by their outer membrane-embedded β-barrel domains. In this study, we use mutational analysis on Ag43 to show that the β-hairpin structure of the fourth and fifth extracellular loops of the β-barrel domain have a crucial role for passenger domain folding and subsequent formation of bacterial aggregates. Mutagenesis of the homologous autotransporter, adhesin involved in diffuse adherence (AIDA-I), suggests that the requirement of these long extracellular loops for passenger folding and biological function is conserved among self-associating autotransporters. This work provides mechanistic insight into the role of the autotransporter β-barrel domain as a folding vector that mediates rapid folding of the passenger domain into the β-helix that enables bacterial interactions during infection.