Cadmium (Cd), a highly toxic and mobile heavy metal, has emerged as a severe environmental concern in global agroecosystems, posing a substantial threat to human health. Although prior studies have established that ZAT6 and ZAT10 positively regulate Arabidopsis tolerance to Cd toxicity, the underlying molecular mechanisms remain largely elusive. The present study provides evidence that a class I TCP transcription factor, TCP9, significantly enhances Arabidopsis tolerance to Cd toxicity through the direct activation of ZAT6 and ZAT10 expression. The real-time quantitative PCR (RT-qPCR) analysis indicates that the expression of TCP9 was induced under Cd toxicity. Meanwhile, the tcp9 mutant exhibited heightened sensitivity to Cd toxicity, accompanied by elevated Cd accumulation in both shoots and roots. Notably, the complemented lines exhibited phenotypic characteristics analogous to those observed in the wild-type (WT) plants. Further physiological and biochemical analyses revealed that, in comparison to WT, the tcp9 mutant displayed elevated hydrogen peroxide (H₂O₂) accumulation and reduced contents of catalase (CAT), ascorbate peroxidase (APX), and peroxidase (POD) under Cd toxicity. Furthermore, TCP9 directly interacted with the promoters of ZAT6 and ZAT10 in vitro, facilitating their transcription and consequently enhancing plant tolerance to Cd toxicity. Overall, our findings showed that TCP9 enhances Cd tolerance via modulating ZAT6 and ZAT10, thereby identifying TCP9 as a potential key target for improving plant tolerance to Cd toxicity.