Internalisation of the pathogenic bacterium Listeria monocytogenes involves interactions between the invasion protein InlB and the hepatocyte growth factor receptor, Met. Using colocalisation studies, dominant-negative constructs and small interfering RNA (siRNA), we demonstrate a cell-type-dependent requirement for various WASP-related proteins in Listeria entry and InlB-induced membrane ruffling. The WAVE2 isoform is essential for InlB-induced cytoskeletal rearrangements in Vero cells. In HeLa cells, WAVE1, WAVE2 and N-WASP cooperate to promote these processes. Abi1, a key component of WAVE complexes, is recruited at the entry site in both cell types and its inactivation by RNA interference impairs InlB-mediated processes. Ena/VASP proteins also play a role in Listeria internalization, and their deregulation by sequestration or overexpression, modifies actin cups beneath entering particles. Taken together, these results identify the WAVE complex, N-WASP and Ena/VASP as key effectors of the Met signalling pathway and of Listeria entry and highlight the existence of redundant and/or cooperative functions among WASP-family members.