The intestinal lymphatic system provides two vital processes to maintain physiologic equilibrium, its modulation of immune tolerance and absorption of dietary lipids. Pathologic defects in intestinal lymphatic vessels can lead to increased fluid retention and immune dysregulation, which ultimately impairs organ physiology. Lymphatic-associated pathologies have been implicated in the etiology of Inflammatory Bowel Diseases (IBD) for almost a century. Despite this, we currently understand very little about how these lymphatic defects contribute to the establishment and progression of Crohn’s Disease (CD) and Ulcerative Colitis (UC). Therefore, we chose to evaluate lymphatic gene expression along the continuum of disease in TNFΔARE+/- Crohn’s-like ileitis and CD4+CD45RBhigh Rag1-/- T cell transfer mediated colitis models. A reduction in lymphatic endothelial cell (LEC) identity signatures prox1, sox18 and lyve1, corresponded with an increase in colitogenic Th1/17-associated cytokines, tnf, lta, ltb, ifng, il17. We also demonstrated this impaired LEC identity signature was also present in a treatment-naïve Irish cohort of paediatric patients with UC. Using primary HDLECs in vitro cultures, we chose to assess the impact of IBD-associated Type 1, Type 2 and Type 17 cytokines on LEC identity, lymphangiogenic, remodeling and structural integrity gene expression profiles. Of note, TNF-α consistently repressed PROX1 and LYVE1 mRNA and induced remodeling FOXC2 transcripts in a time and dose-dependent manner. Through bulk RNA sequencing and pharmacologic inhibition studies we identified TNF-responsive signaling pathways implicated in this transcriptional remodeling pattern, including TNF-α- mediated changes in mTORC1 negative regulation and augmented PROX1 expression loss upon dual TNF-α and Everolimus treatment. This correlated with altered HDLECs morphology post-treatment. Collectively, our data supports the convergence of TNF-α driven loss of PROX1 across in vitro HDLECs culture systems, IBD murine model tissues and patient biopsies and supports the possibility that TNF-α-mTORC1 crosstalk may underpin lymphatic vasculature dysfunction during chronic intestinal inflammation.