Many invasive plant species have demonstrated a greater capacity for tolerating and accumulating heavy metals than their co-occurring native plants. Given the potential biological toxicity associated with metal accumulation in plants and its ability to alter the composition of plant-associated microbial communities, we postulated that heavy metal contamination could potentially enhance the pathogen resistance of metal-accumulating invasive plant species when compared with their local congeneric competitors. This study focused on examining the resistance of the invasive weed Alternanthera philoxeroides and its native congener Alternanthera sessilis to infection by a leaf pathogenic fungus under soil cadmium (Cd) pollution. The findings revealed that despite the detrimental effects of Cd exposure on the growth of both plant species, A. philoxeroides exhibited superior growth and accumulated higher concentrations of Cd in its leaves compared to A. sessilis. Cd stress reduced leaf lesion in both plant species following leaf pathogen infection, with A. philoxeroides experiencing less leaf lesion than A. sessilis. Subsequent analysis of the phyllosphere microbiome and toxicity tests suggested that the increased pathogen resistance of A. philoxeroides following Cd exposure could be attributed to both the direct toxic effects of Cd and the Cd-induced alterations in the microbial composition of the epiphytic phyllosphere. We further isolated a bacterial strain with potent antagonistic properties against the leaf pathogen, potentially elucidating the enhanced pathogen resistance of A. philoxeroides under soil Cd pollution. This study advances our understanding of how heavy metal pollution might augment the pathogen resistance of invasive plants by influencing plant-associated microbial communities.