Using environmental cues, bacteria commit to the assembly of transmembrane complexes such as the type III secretion system 2 (T3SS2), a membrane-bound, syringe-like secretory apparatus used during infection to inject host cells with virulence factors. Here we report Vibrio parahaemolyticus uses transertion, localized transcription, translation, and membrane insertion, to assemble its T3SS2. Upon binding bile acids, the membrane bound receptor and transcription factor VtrA/VtrC captures the T3SS2 pathogenicity island at the inner membrane. Activated VtrA/VtrC induces production of VtrB, the membrane bound master T3SS2 transcriptional regulator. VtrB then induces the membrane-proximal T3SS2 genes to undergo transertion for assembly of the membrane inserted secretion machinery. Transertion is a process that can be used for the efficient assembly of membrane-bound molecular complexes in response to extracellular signals.