Certain pathogenic bacteria produce and release toxic peptides to ensure either nutrient availability or evasion from the immune system. These peptides are also toxic to the producing bacteria that utilize dedicated ABC transporters to provide self‐immunity. The ABC transporter McjD exports the antibacterial peptide MccJ25 in Escherichia coli. Our previously determined McjD structure provided some mechanistic insights into antibacterial peptide efflux. In this study, we have determined its structure in a novel conformation, apo inward‐occluded and a new nucleotide‐bound state, high‐energy outward‐occluded intermediate state, with a defined ligand binding cavity. Predictive cysteine cross‐linking in E. coli membranes and PELDOR measurements along the transport cycle indicate that McjD does not undergo major conformational changes as previously proposed for multi‐drug ABC exporters. Combined with transport assays and molecular dynamics simulations, we propose a novel mechanism for toxic peptide ABC exporters that only requires the transient opening of the cavity for release of the peptide. We propose that shielding of the cavity ensures that the transporter is available to export the newly synthesized peptides, preventing toxic‐level build‐up. Synopsis Bacteria employ dedicated ABC transporters to secrete antibacterial peptides. X‐ray structure analysis shows that the antibacterial lasso peptide transporter McjD, in contrast to other ABC transporters, lacks a stable open cavity conformation, thus preventing the influx of the exported toxic peptide. The structure of the ABC transporter McjD was determined in two distinct conformations, apo and nucleotide‐bound. Both conformations show an occluded cavity at both sides of the membrane. Pulsed electron‐electron double resonance (PELDOR) measurements in the presence of the antibacterial peptide MccJ25 did not identify a stable open‐conformation. Cross‐linking studies in proteoliposomes show that the cavity opens transiently to release the bound substrate. Transient opening of the antibacterial peptide transporter McjD prevents the influx of its toxic substrate MccJ25 and distinguishes it from other multi‐drug transporters.