Iron (Fe) and phosphate (Pi) are essential nutrients for plant growth. Several interactions between Fe and Pi homeostasis have been described, such as the Fe-dependent inhibition of primary root growth under Pi deficiency. This response involves the formation of apoplastic Fe3+-malate complexes in the root meristem which implicates the oxidation of Fe2+ by the LPR1 ferroxidase. However, how the Fe3+/Fe2+ ratio is regulated in the meristem is unknown. We identified a gene in Arabidopsis, named CRR, implicated in primary root growth under Pi deficiency. Under low-Pi conditions, the crr mutant showed enhanced reduction of primary root growth associated with increased accumulation of apoplastic Fe in the meristem and a reduction in cell division. Conversely, CRR overexpression rendered primary root growth insensitive to low-Pi inhibition, reduced root apoplastic Fe, and impacted the expression of genes involved in Fe and redox homeostasis. CRR is a member of an uncharacterized CYBDOM protein family possessing a cytochrome b561 (CYB561) with an N-terminal DOMON domain. CRR localizes to the plasma membrane and possesses ascorbate-dependent ferric reductase activity. The crr single and crr hyp1 double mutant, which harbored a null allele in another CYBDOM gene, showed increased tolerance to high-Fe stress upon germination and seedling growth. In contrast, CRR overexpression was associated with increased uptake and translocation of Fe to the shoot, resulting in plants sensitive to Fe excess. Our results thus identify a novel ferric reductase implicated in root Fe acquisition and homeostasis and reveal a biological role for CYBDOM proteins in plants.