Pseudomonas aeruginosa typically carries three T6SSs, but clinical isolates can harbor an additional H4 system whose function was unknown. Wu et al. show that the H4-T6SS of clinical isolate LYSZa7 is a functional secretion apparatus when transcriptionally activated. They identify TseMt as a major antibacterial effector that acts in the periplasm, binds membranes, and forms ion-conducting pores. A 3.0-A cryo-EM structure reveals a compact three-domain architecture in which membrane-interacting elements are sequestered before activation. Genetic and structural analyses further define a dedicated DUF4123 chaperone-VgrG4b-PAAR4 delivery pathway. The work provides the first functional validation of P. aeruginosa H4-T6SS and mechanistic characterization of an H4-encoded effector.