Epithelial cell adhesion molecule (EpCAM) is a pleiotropic transmembrane glycoprotein comprising an extracellular domain (EpEX), a single transmembrane domain, and an intracellular domain (EpICD). In several types of cancer, high EpCAM expression is associated with tumor progression, metastasis, immune evasion, and poor overall prognosis. Anaplastic thyroid cancer (ATC), a rare but aggressive form of thyroid cancer, has a mean survival time of only 3-6 months after diagnosis. EpEX and EpICD cleavage levels in clinical patient samples were evaluated using a tissue microarray. RNA-seq was conducted, and differential gene expression and gene set enrichment analyses were subsequently performed to identify EpCAM knockout-associated molecular alterations and affected biological pathways. The functions of EpCAM or EpEX in ATC were investigated by proliferation, invasion, and stemness analysis. In this study, we observed that ATC samples typically exhibited a marked loss of membrane EpEX, along with increased nuclear and cytoplasmic accumulation of EpICD, compared with non-ATC samples. Furthermore, we found that EpEX induced phosphorylation of EGFR, HGFR, and Wnt receptors in ATC cells to promote cell growth, invasion, and stemness activity. EpCAM signaling also increases TNF-α expression and induces TNF-α cleavage, clarifying the crosstalk between EpCAM and TNF-α in regulating the ERK-EGR1 axis signaling. Inhibition of EpCAM signaling suppressed regulated intramembrane proteolysis (RIP) of EpCAM and shedding of EpEX and EpICD in ATC cells. Combined treatment of EpAb2-6 and BRAF inhibitor dabrafenib coordinately induced apoptosis, while also inhibiting invasion, stemness, and lung metastasis, and prolonging survival in an animal model of metastatic ATC. This study elucidates the molecular mechanisms by which EpCAM signaling promotes anaplastic thyroid cancer (ATC) tumor progression via the ERK-EGR1-TNF-α axis. Our findings suggest that an EpCAM-neutralizing antibody may enhance the therapeutic efficacy of the BRAF inhibitor dabrafenib in ATC.