Embryonal Tumors with Multilayered Rosettes (ETMR) are a diverse and rare, but highly aggressive, form of embryonal brain tumors. All ETMRs share common histological and transcriptomic traits such as the presence of highly proliferative rosettes and aberrations on relevant miRNAs signaling pathways, including depletion of let-7 family miRNAs and increased Lin28A expression. Two different genetic alterations have been found to underlie ETMR tumors: amplification of the C19MC microRNA cluster, and biallelic Dicer1 inactivating mutations. Remarkably, a faithful animal model recapitulating this pathology is still missing. We aimed to generate a mouse line faithfully modeling ETMR, to help unravel the origin and biological nature of these tumors, and to identify valid and specific therapeutic targets. We find that the Rx-Cre;DicerF/F conditional transgenic mouse line, lacking Dicer in early telencephalic progenitor cells, recapitulates many of the distinctive features of ETMR tumors, particularly the formation of proliferative rosettes. Focusing on the early onset and late progression of this phenotype, our immunohistochemical and bulk RNA-seq analyses reveal the formation of ETMR-like rosettes in septal and rostral cortical regions, with transcriptomic similarities such as increased p53 signaling, decreased let-7 family miRNAs and increased Lin28A expression. ETMR signature genes such as IRS1, Lin28A/B and PRTG were also overexpressed in Rx-Cre;DicerF/F mutants, and our experiments show that their individual overexpression by in utero electroporation is sufficient to drive the formation of proliferative rosettes in wild-type mouse embryos. Altogether, our findings reveal Rx-Cre;DicerF/F mice as the only faithful animal model of ETMR.