Metabonomics in inflammatory bowel disease (IBD) characterizes the effector molecules of biological systems and thus aims to describe the molecular phenotype, generate insight into the pathology, and predict disease course and response to treatment. Nuclear magnetic resonance (NMR) spectroscopy, mass spectrometry (MS), and integrated NMR and MS platforms coupled with multivariate analyses have been applied to create such metabolic profiles. Recent advances have identified quiescent ulcerative colitis as a distinct molecular phenotype and demonstrated metabonomics as a promising clinical tool for predicting relapse and response to treatment with biologics as well as fecal microbiome transplantation, thus facilitating much needed precision medicine. However, understanding this complex research field and how it translates into clinical settings is a challenge. This review aims to describe the current workflow, analytical strategies, and associated bioinformatics, and translate current IBD metabonomic knowledge into new potential clinically applicable treatment strategies, and outline future key translational perspectives.