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Inflammatory bowel disease (IBD) manifests systemically, yet most comorbidity studies rely on predominantly European populations. The All of Us Research Program enables investigation across demographically diverse groups. We matched 5,094 IBD patients 1:4 with controls by age, gender, and race, analyzing comorbidities using logistic regression with Mantel–Haenszel adjustment. Multiple testing correction used false discovery rate (FDR) with significance thresholds of OR > 1.5 or < 0.5 and FDR < 0.05. Our cohort included 29.2% non-White participants versus 10–15% in traditional studies. We identified 22 significant associations across seven organ systems. Three novel discoveries included delayed postmyocardial infarction pericarditis (adjusted OR = 4.80), contact dermatitis (adjusted OR = 1.84), and carotid artery aneurysm (adjusted OR = 2.21). Other significant associations included drug-induced lupus (adjusted OR = 4.32), autoimmune hepatitis (adjusted OR = 2.43), and anorexia nervosa (adjusted OR = 2.29). IBD patients showed decreased obesity-related conditions. This demographically diverse study discovered novel IBD comorbidities and confirmed established associations across racial groups. Findings support conceptualizing IBD as a multisystem disorder requiring comprehensive management and demonstrate the importance of diverse research populations. • What is already known? IBD patients have increased risk of autoimmune, dermatologic, and cardiovascular comorbidities, but most studies focus on predominantly White European populations with limited demographic diversity. • What is new here? This large, demographically diverse IBD study (29.2% non-White participants) identified three novel associations: delayed postmyocardial infarction pericarditis, contact dermatitis, and carotid artery aneurysms across 22 significant comorbidities spanning seven organ systems. • How can this study help patient care? These findings support implementing multidisciplinary IBD care with enhanced cardiovascular monitoring post-myocardial infarction, systematic dermatologic screening, and updated surveillance protocols addressing newly identified systemic manifestations.