Dynamic coordination of energy metabolism and protein synthesis is pivotal to cell fitness, especially in cancer cells facing microenvironmental challenges. Whether this rapid communication depends on complex signaling pathways or can be mediated by a single molecule remains unclear. Here, we show that intracellular accumulation of lactate, a central glycolytic product, is sufficient to acutely repress mRNA translation. Mechanistically, lactate is charged to tRNA aminoacylation sites instead of amino acids by AARS1. The slower charging kinetic of lactate extends lactylation to non-cognate tRNAs, further exacerbating translation repression. This direct metabolic control over the central dogma may function to restrict protein synthesis during metabolic imbalance, yet, cancer cells evade this brake by enhancing lactate export to sustain pro-tumor translation. Pharmacological blockade of lactate export re-establishes translational repression and impairs tumor progression. These findings uncover a unique metabolite-tRNA charging event directly rewiring translational output and reveal a metabolic vulnerability with therapeutic potential.