γδ T cells have evolved as a third lymphocyte lineage alongside αβ T cells and B cells over millions of years of vertebrate evolution1. Human gd T cells constitute only a small proportion of all the circulating T lymphocytes in the blood but are enriched at mucosal barriers2. Inflammatory bowel disease (IBD), which includes ulcerative colitis (UC) and Crohn’s disease (CD) is thought to involve a dysregulated response from the mucosal immune system to the intestinal microbiota resulting in chronic inflammation of the gastrointestinal tract3. Here, we investigated the dynamics of human paediatric gd T cell subsets in the intestinal tissue and circulation at the early stages of IBD. Using immunophenotyping and T cell receptor (TCR) repertoire profiling we found that children at the first diagnosis of IBD displayed clonal populations of Vd1+ TCRs in the blood compared to age and gender matched healthy children. Moreover, circulating Vd1+ T cells in IBD children had shifted their phenotype from a CD27+ CD28+ naïve-like population to a cytotoxic CD27neg effector population. We then explored the relationship of circulating and intestinal resident populations of Vd1+ T cells. Firstly, we found that expanded Vd1+ T cell clonotypes in circulation, duodenum, terminal ileum and rectum contained unique tissue-location dependent TCR repertoires. Secondly, chronic Crohn’s disease associated inflammation drove the remodelling of terminal ileum resident Vd1+ T cells. Our study indicates that tissue-resident Vd1+ T cells in discrete niches of the intestine display unique TCR repertoires. Morevoer, the onset of IBD has a major impact on intestinal and circulating populations of Vd1+ T cells. These findings show that the γδ T cell repertoire is highly responsive to the early stages of chronic intestinal inflammation