Dysregulation of RNA modifications is increasingly implicated in tumorigenesis. This study identifies TRMT6, the catalytic subunit of the tRNA m1A58 methyltransferase complex, as being significantly upregulated in breast cancer (BC). High TRMT6 expression correlates strongly with advanced tumor stage and poor patient prognosis. We demonstrate that TRMT6 overexpression elevates global tRNA m1A methylation levels. Mechanistically, TRMT6-dependent m1A modification on specific tRNAs, particularly those decoding the start codon and specific amino acids, selectively enhances the translation efficiency of mRNAs encoding the iron storage proteins FTH1 and FTL1 (Ferritin Heavy and Light Chains), confirmed by polysome profiling and Ribo-seq. Consequently, this leads to dysregulated cellular iron homeostasis and a profound suppression of ferroptosis – an iron-dependent, lipid peroxidation-driven cell death pathway critical for tumor suppression. Functional studies show that TRMT6 knockdown significantly reduces FTH1/FTL1 protein levels, increases lipid peroxidation, and sensitizes BC cells to ferroptosis inducers in vitro, while potently inhibiting tumor growth and metastasis in vivo. Conversely, TRMT6 overexpression confers robust resistance to ferroptosis. Collectively, our results uncover a novel oncogenic axis where TRMT6 drives BC progression via tRNA m1A modification-dependent enhancement of FTH1/FTL1 translation and subsequent ferroptosis evasion, positioning TRMT6 as a promising therapeutic target for overcoming ferroptosis resistance in breast cancer.