Streptococcus pneumoniae is the world's foremost bacterial pathogen. It is responsible for more than 1 million deaths every year and kills more children than AIDS, malaria and tuberculosis combined. Human zinc deficiency compromises immune defence and increases susceptibility to bacterial infection. Although clinical trials have shown that the morbidity and mortality of pneumococcal pneumonia can be significantly reduced by zinc supplementation therapies, the efficacy of supplementation therapies vary, highlighting that the underlying mechanisms of how zinc contributes to host resistance to infection remain unclear. To address this, we combined a murine model of dietary zinc restriction with elemental bio-imaging, mutant S. pneumoniae strains and molecular analyses of the host-pathogen responses to ascertain how host zinc abundance influences pneumococcal infection. Here, we show that dietary zinc restricts colonisation by S. pneumoniae in a murine model of pneumococcal disease and improves survival times post-infection. Analyses of tissue metal content reveal that host zinc is redistributed during pneumococcal infection, although this is both niche-specific and influenced by host zinc status. Zinc directly impacts S. pneumoniae during infection, with bacterial transcriptional profiling showing dysregulation of manganese and zinc homeostasis. Although zinc is implicated in having broad roles in immune function, we observed that differences in host zinc status had no significant effect on the infiltration of the immune cells or upon immune activation during infection. Despite this, examination of cellular zinc levels reveals that dietary zinc restriction affects the zinc status of host phagocytic cells and their ability to kill S. pneumoniae. Hence, this work directly links dietary zinc intake, with the ability of phagocytic cells to effectively kill bacteria via zinc toxicity. This work provides a robust basis for the use of zinc supplementation therapies as a disease prevention strategy in groups at increased risk of contracting S. pneumoniae infections.