Inflammatory bowel disease (IBD) results from a dysregulated interaction between the microbiota and a genetically susceptible host. Genetic studies have linked TNFSF15 polymorphisms and its protein TNF-like ligand 1A (TL1A) with IBD, but the functional role of TL1A in linking tissue homeostasis and intestinal inflammation is not known. Here, using cell-specific genetic deletion models, we report an essential role for CX3CR1+ mononuclear phagocyte (MNP) TL1A in signaling through its cognate receptor death receptor 3 (DR3) on group 3 innate lymphoid cell (ILC3) to promote IL-22 dependent protection during acute colitis. Induction of intestinal MNP TL1A by IBD-associated adherent microbes confers TL1A-dependent protection from acute colitis. However, in contrast to this protective role in acute colitis, colitis- induced DR3-dependent expression of OX40L enables MHCII+ ILC3 to co-stimulate antigen-specific T cell proliferation and exacerbate chronic T cell- dependent colitis. Colonic biopsies from IBD patients revealed increased TL1A expression on MNPs and OX40L on ILC3 compared to healthy controls, highlighting the conserved TL1A-OX40L ILC3 axis in IBD. These results identify the mechanistic contributions of this IBD-linked pathway as a central regulator of ILC3 function in tissue homeostasis.