Manganese (Mn) toxicity poses a severe hazard to plant growth, with organic acids playing a crucial role in detoxifying toxic metals. However, the regulatory mechanisms governing the response of organic acids to Mn toxicity remain largely elusive, particularly in perennial fruit crops. Herein, we investigated the physio-biochemical and transcriptomic responses of peach seedlings to Mn toxicity. Organic acids, especially malate, significantly increased in Mn-treated peach seedlings. Subsequently, malate application markedly mitigated Mn toxicity in peach. Further, we identified a key vacuolar malate transporter, PpTDT, whose expression was dramatically induced by both Mn and malate treatments. PpTDT was localised to the vacuolar membrane. Heterologous expression of PpTDT in yeast restored growth arrest and enhanced Mn tolerance. Overexpression of PpTDT in tobacco, peach leaves and roots enhanced Mn toxicity tolerance, and increased malate and Mn content. Conversely, silencing of PpTDT in peach seedlings exacerbated Mn toxicity, resulting in decreased malate and Mn content. These findings unveil the role of PpTDT in facilitating intracellular chelation of Mn through malate transport, thereby imparting Mn toxicity tolerance in peach. Our study also highlights the potential of malate as an natural compound for improving Mn toxicity tolerance in peach and potentially other fruit crops.