While several studies have documented associations between dietary habits and microbiota composition and function in healthy individuals, no study explored these associations in patients with irritable bowel syndrome (IBS), and especially with symptoms. Here, we used a novel approach that combined data from a 4-day food diary, integrated into a food tree, together with gut microbiota (shotgun metagenomic) for individuals with IBS ( N = 149) and healthy controls ( N = 52). Paired microbiota and food-based trees allowed us to detect new associations between subspecies and diet. Combining co-inertia analysis and linear regression models, exhaled gas levels and symptom severity could be predicted from metagenomic and dietary data. We showed that individuals with severe IBS are characterized by a higher intake of poorer-quality food items during their main meals. Our analysis suggested that covariations between gut microbiota at subspecies level and diet could be explained with IBS symptom severity, exhaled gas, glycan metabolism, and meat/plant ratio. We provided evidence that IBS severity is associated with altered gut microbiota hydrogen function in correlation with microbiota enzymes involved in animal carbohydrate metabolism. Our study provides an unprecedented resolution of diet-microbiota-symptom interactions and ultimately guides new interventional studies that aim to identify gut microbiome-based nutritional recommendations for the management of gastrointestinal symptoms.