The Type VI secretion system (T6SS) is a multiprotein weapon used by bacteria to destroy competitor cells. The T6SS belongs to the broad family of contractile injection systems (CIS) that require a spring-like tail to propel a needle loaded with effectors. Usually, CIS length is strictly controlled by a dedicated protein called tape-measure protein (TMP). Although no gene encoding a potential TMP can be found within T6SS clusters, we observed that the length of the T6SS tail is constant in enteroaggregative Escherichia coli cells, suggesting that it is strictly controlled. By using fluorescence microscopy, we first demonstrate that tail component stoichiometry does not participate to the regulation of tail length. The observation of longer T6SS tails when the apparatus is relocalized at the cell pole further shows that tail length is not controlled by a tape-measure protein as seen in contractile bacteriophages. We also show that the tail stops its elongation when in contact with the opposite membrane, and thus that T6SS tail length is determined by the cell width acting as a physical ruler. To get insights about the molecular mechanism occurring at the opposite membrane to stop T6SS tail elongation, we adapted an assay based on APEX2-dependent biotinylation to identify the proximity partners of TssA, the cap protein that plays a central role in coordinating the polymerization of the tail at its distal extremity. This approach revealed a new T6SS protein, TagA. We showed that TagA is a cytosolic protein tightly associated with the membrane. By using fluorescence microscopy, we finally determined that TagA acts as the T6SS tail stopper: it captures the distal end of the sheath once the polymerization is completed and maintains the sheath under the extended conformation to prevent unfruitful contraction events.