MET amplification as a mechanism of acquired resistance to EGFR targeted therapies in non-small cell lung carcinoma (NSCLC) led to investigation of novel combinations of EGFR and MET kinase inhibitors. However, promiscuous interactions between MET and ERBB family members have made it difficult to evaluate the effects of MET on EGFR signaling, both independent of drug treatment and in the context of drug resistance. We addressed this issue by establishing a 32D model cell system wherein ERBBs or MET are expressed alone and in combination. Using this model, we determined that EGFR signaling is sufficient to induce MET phosphorylation, although MET activation is enhanced by co-expression of ERBB3. EGFR-MET crosstalk was not direct but occurred by a combined regulation of MET levels and intermediary signaling through MAP kinases. In NSCLCs harboring either wild-type or mutant EGFR, inhibiting EGFR or MAP kinases reduced MET activation and protein levels. Furthermore, MET signaling promoted EGFR-driven migration and invasion. Lastly, EGFR-MET signaling was enhanced in a highly metastatic EGFR mutant cell subpopulation, compared to the indolent parental line, and MET attenuation decreased the incidence of brain metastasis. Overall, our results establish that EGFR-MET signaling is critical for aggressive behavior of NSCLCs and rationalize its continued investigation as a therapeutic target for tumors harboring both wild-type and mutant EGFR at early stages of progression.