Merkel cell carcinoma (MCC) is a highly aggressive skin cancer that lacks biomarkers for early detection of metastatic disease and effective treatment options for advanced disease. In this study, we investigated the clinical significance and functional role of Insulin-like growth factor 2 mRNA-binding protein 3 (IGF2BP3), an RNA binding protein involved in tumorigenesis and tumor progression, in MCC. Our results revealed that IGF2BP3 expression was significantly elevated in MCC metastases compared to primary tumors. Moreover, its higher level was also associated with shorter disease-specific survival. Using an MCC xenograft model, we observed increased IGF2BP3 expression in lung metastases, and its higher expression in primary tumors correlated with a greater propensity for lung metastasis. Employing gain- and loss-of-function experiments, we established the pivotal role of IGF2BP3 in regulating cell migration and invasion in MCC. RNA immunoprecipitation sequencing analysis identified 281 RNA targets of IGF2BP3. Notably, several of these targets are involved in cell migration, cytoskeleton organization and focal adhesion. Interestingly, some of these targets overlap with differentially expressed genes between primary tumors and metastases in MCC, suggesting that IGF2BP3 and its targets contribute to tumor progression. Furthermore, we identified BRD4 as a potential transcriptional regulator of IGF2BP3. Inhibiting BRD4 not only reduced IGF2BP3 expression but also induced cell death in MCC. In summary, our study sheds light on the involvement of IGF2BP3 in MCC tumor metastasis, highlights its potential as a prognostic biomarker, and provides insights into the molecular mechanism underlying MCC progression.