A high fat (HF) diet decreases levels of Akkermansia muciniphila in the gut and reduces resistance to the foodborne pathogen Listeria monocytogenes. We demonstrate that short-term gavage with A. muciniphila increases resistance to oral and systemic L. monocytogenes infection in mice fed a HF diet. A. muciniphila normalized diet-induced inflammation in the gut and liver prior to infection and reduced inflammatory cell infiltration in the ileum to levels similar to mice fed a low fat diet. A. muciniphila administration had minimal impact upon the microbiota and microbial metabolites and did not affect individual taxa or impact the Bacteroidetes to Firmicutes ratio. In summary, A. muciniphila increased resistance to L. monocytogenes infection in mice fed a HF diet, through normalising immune/physiological effects that more closely resembled mice fed a LF diet. The findings suggest an interaction between A. muciniphila and the host to reverse the effects of a westernized diet in this model.