Invasive carcinoma cells form actin rich matrix-degrading protrusions called invadopodia. These structures resemble podosome produced by some normal cells and play a crucial role in extracellular matrix remodeling. In cancer, formation of invadopodia is strongly associated with invasive potential. Although deregulated signals from the Met receptor tyrosine kinase are linked to cancer metastasis and poor prognosis, its role in invadopodia formation is not known. Here we show that stimulation of breast cancer cells with the ligand for Met, hepatocyte growth factor, promotes invadopodia formation, and in aggressive gastric tumor cells where Met is amplified, invadopodia formation is dependent on Met activity. We show that Met mediated invadopodia formation and cell invasion requires the scaffold protein Gab1, using both Gab1-null fibroblasts and specific knock-down of Gab1 in tumor cells. By a structure function approach, we demonstrate that two proline-rich motifs (p4/5) within Gab1 are essential for invadopodia formation. We identify the actin regulatory protein, cortactin, as a direct interaction partner for Gab1 and show that a Gab1-cortactin interaction is dependent on the SH3 domain of cortactin and the integrity of p4/5 region of Gab1. Both cortactin and Gab1 localize to invadopodia rosettes in Met transformed cells and the specific uncoupling of cortactin from Gab1 abrogates invadopodia biogenesis and cell invasion downstream from the Met RTK. Met localizes to invadopodia along with cortactin and promotes phosphorylation of cortactin. These findings provide novel insights into the molecular mechanisms of invadopodia formation and identify Gab1 as a scaffold protein involved in this process.