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<i>Akkermansia muciniphila</i> (<i>A. muciniphila</i>) and its derivatives, including extracellular vesicles (EVs) and outer membrane proteins, are recognized for enhancing intestinal balance and metabolic health. However, the mechanisms of <i>Akkermansia muciniphila</i>’s action and its effects on the microbiome are not well understood. In this study, we examined the influence of <i>A. muciniphila</i> and its derivatives on gastrointestinal (GI) and metabolic disorders through a meta-analysis of studies conducted on mouse models. A total of 39 eligible studies were identified through targeted searches on PubMed, Web of Science, Science Direct, and Embase until May 2024. <i>A. muciniphila</i> (alive or heat-killed) and its derivatives positively affected systemic and gut inflammation, liver enzyme level, glycemic response, and lipid profiles. The intervention increased the expression of tight-junction proteins in the gut, improving gut permeability in mouse models of GI and metabolic disorders. Regarding body weight, <i>A. muciniphila</i> and its derivatives prevented weight loss in animals with GI disorders while reducing body weight in mice with metabolic disorders. Sub-group analysis indicated that live bacteria had a more substantial effect on most analyzed biomarkers. Gut microbiome analysis using live <i>A. muciniphila</i> identified a co-occurrence cluster, including <i>Desulfovibrio</i>, <i>Family XIII AD3011</i> group, and <i>Candidatus Saccharimonas</i>. Thus, enhancing the intestinal abundance of <i>A. muciniphila</i> and its gut microbial clusters may provide more robust health benefits for cardiometabolic, and age-related diseases compared with <i>A. muciniphila</i> alone. The mechanistic insight elucidated here will pave the way for further exploration and potential translational applications in human health.