Abstract Objectives Peri-bowel fat inflammation is a prominent feature of inflammatory bowel disease (IBD). The peri-bowel fat attenuation index (FAI) can capture fat inflammation on abdominal CT. This study aimed to investigate the prognostic value of the peri-bowel FAI in IBD patients. Materials and methods Totally, 207 IBD patients were retrospectively collected. Regions of interest were placed at 5 different locations, namely, mesenteric side (MS) and opposite side of MS (OMS) around the most severe bowel lesion, spaces around the normal bowel wall (Nor), retroperitoneal space (RS), and subcutaneous area. The Kaplan–Meier curves were plotted. The prognostic value of the peri-bowel FAI was evaluated by multivariable Cox regression models. Results High peri-bowel FAI values of MS and OMS were predictors of disease progression and correlated strongly with each other (r = 0.840, p < 0.001), while the FAI of Nor and RS were not. Therefore, peri-bowel FAI of MS was used as a representative biomarker for the prediction of IBD disease progression (HR = 1.161 [1.110–1.215], p < 0.001) with an optimum cutoff of 25.1 HU, which was confirmed in the subgroup analysis with different disease subtypes. With the addition of the peri-bowel FAI to the current noninvasive risk prediction model, the AUC increased from 0.706 (0.638–0.767) to 0.864 (0.810–0.90) with integrated discrimination improvement (IDI = 0.293 [0.229–0.356], p < 0.001) and net reclassification improvement (NRI = 1.053 [0.821–1.284], p < 0.001). Conclusion The peri-bowel FAI is promising for IBD disease progression prediction and risk stratification by quantifying peri-bowel fat inflammation. High peri-bowel FAI values are an independent indicator of increased IBD disease progression and could guide early targeted prevention and intensive therapy. Key Points Questions The peri-bowel fat attenuation index (FAI) helps detect peri-bowel fat inflammation noninvasively, but its importance for risk stratification and prediction of clinical outcomes remains unknown. Findings The peri-bowel FAI was an independent predictor of inflammatory bowel disease (IBD) disease progression with an optimum cutoff of 25.1 HU. Clinical relevance The peri-bowel FAI is a promising biomarker for contributing to the identification of so-called high-risk patients with uncontrolled inflammation, who might be candidates for more intensive treatment for addressing underlying inflammation at early stages and ultimately improve long-term prognosis. Graphical Abstract