Cadmium (Cd) is a highly toxic element that is easily absorbed by plant, and the mechanisms of the plant response to Cd toxicity are very complex. In this study, the role of LPR1 (LOW Phosphate Root 1) encoding a cell-wall-targeted ferroxidase in Cd stress was investigated. The results showed that the overexpression of LPR1 caused an average reduction of 23%–40% in the primary root lengths, 67%–73% in the fresh weights, 32%–46% in the lengths of the non-root hair zone (NRHZ) and 70%–71% in the chlorophyll contents in both LPR1-OX lines when compared with the wild type (WT), while there were no significant changes in these traits between the WT and mutant lpr1 lines under Cd stress (7.5 μmol/L CdSO₄). Further investigation showed that the overexpression of LPR1 triggered reactive oxygen species (ROS) bursts and reduced the entry of available iron (Fe²⁺) into the cell, which induced the expression of iron-regulated transporter 1 (IRT1). The up-regulation of IRT1 contributed to the increase of Cd accumulation and growth retardation under Cd stress. Exogenous Fe and ROS scavengers down-regulated the IRT1's expression and alleviated the growth inhibition in LPR1-OX lines, indicating that LPR1-dependent ROS up-regulated IRT1, which subsequently exacerbated the Cd influx into plants. Our findings highlight a pathway of LPR1-mediated plant responding to Cd toxicity stress through the regulation of ROS and Fe homeostasis.