The lymphatics have emerged as critical players both in the progression and resolution of inflammation. The goal of this study was to identify specific microRNAs (miRNAs) that regulate lymphatic inflammatory processes. Rat mesenteric lymphatic endothelial cells (LECs) were exposed to the proinflammatory cytokine tumor necrosis factor-α (TNF-α) for different time points (2hr, 24hr and 96hr) and miRNA profiling was carried out by Real time PCR arrays. Our data demonstrate a specific set of miRNAs that are differentially expressed (>1.8 fold and/or p<0.05) in LECs in response to TNF-α and are involved in inflammation, angiogenesis, endothelial to mesenchymal transition (EndMT), cellular proliferation and senescence. We further characterized the expression of miR-9 that was induced in LECs and in inflamed rat mesenteric lymphatics. Our results showed that miR-9 overexpression, significantly repressed NF-B expression, thereby suppressing inflammation but promoted LEC tube formation as well as the expression of the pro-lymphangiogenic molecules eNOS and VEGFR3. LEC viability, proliferation and EndMT were also significantly induced by miR-9. This study provides the first evidence of a distinct profile of miRNAs associated with LECs during inflammation. It also identifies the critical dual role of miR-9 in fine-tuning the balance between lymphatic inflammatory and lymphangiogenic pathways.