The phytodegradation of emerging phenolic pollutants (EPPs) has attracted widespread attention. However, the impact of bromide ions (Br−) on the phytodegradation of EPPs and its mechanism mediating wheat resistance to EPPs stress have rarely been reported. Our research discovered that Br− enhanced the removal of EPPs (7.5, 15 mg/L) in a dark hydroponic wheat system. The degradation efficiency of acetaminophen (ACE), bisphenol A (BPA) and 1-naphthol (1-NP) increased 2.2, 2.8 and 1.28 times as Br− concentration increased from 0 to 1 mM, respectively. In the presence of Br−, the mono- and dibromo-products of ACE and BPA were produced in the dark hydroponic wheat system, while 1-NP showed higher degradation efficiency but no bromine substitution formation. EPPs induced oxidative damage and root growth inhibition in wheat. The addition of Br− enhanced the chlorophyll content, indole-3-acetic acid (IAA) content and antioxidant potential to alleviate EPPs stress. Principal component analysis (PCA) revealed significant separation of different Br− stimuli, that is, the low concentrations of Br− (0.1 mM) enhanced the content of IAA by 28.6%, while higher concentrations of Br− (0.5, 1 mM) alleviated membrane lipid peroxidation by improving peroxidase (POD) activity. This is the first report that Br− could stimulate the synthesis of IAA via indole acetonitrile (IAN) pathway and hydrolysis of IAA-conjugates. This study provides more support for the feasibility of phytoremediation techniques for phenolic pollutants and references for the assessment of ecological risks and health hazards of EPPs.