•Fucoidan reduces systematic inflammation and attenuates MetS in HFD-fed mice.•Fucoidan increases Akkermansia population in the gut microbiota of mice with MetS.•Fucoidan ameliorates MetS in association with a robust modulation of gut microbiota. Emerging evidence shows that dietary fucoidan contribute to the prevention and treatment of diverse diseases. Here, using a mouse model, we first demonstrate a similar beneficial effect of two fucoidans from Laminaria japonica and Ascophyllum nodosum on diet-induced metabolic syndrome (MetS). Both fucoidans were found to significantly reduce body weight, fasting blood glucose, hepatic steatosis and systematic inflammation. To decipher the mechanism behind this therapeutic effect, the gut microbiota was analyzed as fucoidan is poorly absorbed after oral administration. Interestingly, we found that benign microbes which conferred benefits upon host wellbeing including Akkermansia muciniphila and short-chain fatty acid-producers such as Alloprevotella, Blautia and Bacteroides were highly enriched by fucoidans. Collectively, our study illustrates a novel application of fucoidan as an anti-MetS functional food and, from a gut microbiota perspective, sheds new insight into the mechanism by which unabsorbed polysaccharide exerts a system therapeutic effect.