<p><i>Erwinia amylovora</i>, a Gram-negative bacterium in the genus <i>Erwinia</i>, responsible for fire blight in rosaceous plants, has long been studied for its aerial infection pathways. However, the root-mediated transmission of <i>E. amylovora</i> remains enigmatic. This study bridges this critical knowledge gap through integrated greenhouse and field experiments on two model systems, i.e. seed-propagated potted birch-leaf pear (<i>Pyrus betulaefolia</i>) sapling in a greenhouse and grafted Korla fragrant pear (<i>Pyrus sinkiangensis</i>) trees using two-year-old birch-leaf pears as the rootstocks in orchards located in Xinjiang, China, as <i>P. betulaefolia</i> exhibits low heterogeneity and high homogeneity. By combining controlled root wounding regimes (fibrous roots/lateral roots/taproots) and soil drenching or embedded <i>E. amylovora</i>-infected branches, we found that taproot-wounded specimens exhibited higher disease incidence (57.4% ± 3.1%) than lateral root- (34.4% ± 2.1%) and fibrous root-wounded (12.3% ± 0.6%) specimens with 10⁸&#xa0;CFU/mL <i>E. amylovora</i> suspension at 15 dpi. Field trenching trials demonstrated depth-dependent epidemiology, and 40-cm deep tillage compromising taproots (30 − 40&#xa0;cm) caused significant disease incidence versus 0% disease incidence in 20-cm trenching. Based on the findings, we proposed a root-aware tillage protocol, including controlling restrict depth (shallow depth ≤ 20&#xa0;cm to protect taproots, or deep depth &gt; 40&#xa0;cm using vertical-shank subsoilers), and implementing dormancy-phase operations to leverage accelerated wound healing. Overall, this study not only first provided robust evidence demonstrating that <i>E. amylovora</i> can infect pear plants through the root system in China but also offered practical guidance for establishing fire blight-free cultivation practices in fragrant pears.</p>