Lung fibroblasts play a pivotal role in pulmonary fibrosis, a devastating lung diseases, by producing extracellular matrix. MicroRNAs (miRNAs) suppress a lot of genes posttranscriptionally, but the dynamics and the role of miRNAs in activated lung fibroblasts in fibrotic lung has been poorly understood. To elucidate these problems, we performed global miRNA expression profiling of lung fibroblasts of bleomycin- and silica-induced fibrotic lungs, and investigated the functions of miRNAs in activated lung fibroblasts both in vitro and in vivo. Clustering analysis of global miRNA expression data identified the miRNA signatures of which expression increased as the fibrosis progression. Among these miRNA signatures, we found miR-19a,19b,20a cluster, one of the member of the miRNA signatures, suppressed transforming growth factor(TGF)-β-induced activation signatures of fibroblasts in vitro. Moreover, to elucidate whether fibroblast-specific intervention against miR-20a modulates pathogenic activation of lung fibroblasts in vivo, we intratracheally-transferred miR-19a,19b,20a cluster-overexpressed fibroblasts into bleomycin-treated lungs. Global transcriptome analysis of the intratracheally-transferred fibroblasts revealed that miR-19a,19b,20a cluster not only downregulated expression of TGF-β-associated profibrotic genes, including Acta2, Col1a1, Ctgf, and Serpine1, but also upregulated expression of anti-fibrotic gene Dcn, Igfbp5 and Mmp3 in activated lung fibroblasts in vivo. Collectively, these findings indicate that upregulation of miR-19a,19b,20a cluster expression in lung fibroblasts counteracts their TGF-β-associated pathogenic activation in murine pulmonary fibrosis.