Salmonella enterica is an intracellular pathogen that causes a range of diseases from gastroenteritis to systemic typhoid fever. Its pathogenesis relies on virulence proteins known as effectors that are delivered into host cells and modulate host cellular processes. The ability of the Salmonella effector SteD to localise within host MHCII compartment membranes is essential for its function in disrupting the adaptive immune response. Here we show that SteD integrates into membranes of the early secretory pathway through a two-step recruitment and integration mechanism. SteD then behaves like a transmembrane cargo protein and hijacks a post-Golgi vesicular trafficking pathway to reach MHCII compartments. This study highlights the sophistication by which bacterial pathogens interact with host cell biology at the molecular level.