Ubiquitination is a crucial posttranslational modification in eukaryotes that plays a significant role in the infection of intracellular microbial pathogens, such as Legionella pneumophila, the bacterium responsible for Legionnaires' disease. While the Legionella-containing vacuole (LCV) is coated with ubiquitin (Ub), it avoids recognition by autophagy adaptors. In this study, we report that the Sdc and Sde families of effectors work together to build ubiquitinated species around the LCV. The Sdc effectors catalyze canonical polyubiquitination directly on host targets or on the phosphoribosyl-Ub (PR-Ub) conjugated to host targets by Sde. Remarkably, the Ub moieties within the poly-Ub chains are either modified with a phosphoribosyl group by Sde and other PDE domain-containing effectors or covalently attached to other host substrates via Sde-mediated PR-ubiquitination. Furthermore, these modifications prevent the recognition by Ub adaptors, such as p62, and therefore exclude host autophagy adaptors from the LCV. Our findings shed light on the nature of the poly-ubiquitinated species present at the surface of the LCV and provide a molecular mechanism for the avoidance of autophagy adaptors by the Ub-decorated LCV.