The oncofetal IGF2 mRNA-binding protein 1 (IGF2BP1) controls the migration and invasiveness of different cell types in vitro by regulating the fate of target mRNAs at the post-transcriptional level. Whether the protein is also involved in epithelial-mesenchymal-transition (EMT), a hallmark of cancer progression, remained elusive. In this study, it was disclosed that IGF2BP1 sustains and/or promotes mesenchymal-like cell properties of non-tumor- and tumor-derived cells by enhancing the expression of the transcription factor LEF1. IGF2BP1 directly associates with LEF1 mRNAs and prevents their degradation. The elevated expression of LEF1 in turn up-regulates the transcription of the mesenchymal marker fibronectin (FN1) by associating with its promoter region. Moreover, IGF2BP1 enhances the expression of the EMT-driving factor SNAI2, presumably via LEF1-dependent indirect promoter activation. Accordingly, IGF2BP1 depletion causes MET-like morphological changes with enhanced cell-cell contact formation and decreased cell motility. These findings identify a novel function of IGF2BP1 as a pro-mesenchymal post-transcriptional determinant.