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Abstract Phytophthora root rot, caused by oomycete pathogens in the Phytophthora genus, poses a significant threat to soybean productivity. While resistance mechanisms againstPhytophthora sojaehave been extensively studied in soybean, the molecular basis underlying immune responses toPhytophthora sansomeanaremains unclear. In this study, we investigated transcriptomic and epigenetic responses of two resistant (Colfax and NE2701) and two susceptible (Williams 82 and Senaki) soybean lines at four time points (2, 4, 8, and 16 h post inoculation [hpi]) afterP. sansomeanainoculation. Comparative transcriptomic analyses revealed a greater number of differentially expressed genes (DEGs) upon pathogen inoculation in resistant lines, particularly at 8 and 16 hpi. These DEGs were predominantly associated with defense response, ethylene, and reactive oxygen species‐mediated defense pathways. Moreover, DE transposons were predominantly upregulated after inoculation, and more of them were enriched near genes in Colfax than other soybean lines. Notably, we identified a long non‐coding RNA (lncRNA) within the mapped region of the resistance gene that exhibited exclusive upregulation in the resistant lines after inoculation, potentially regulating two flankingLURP‐one‐relatedgenes. Furthermore, DNA methylation analysis revealed increased CHH (where H = A, T, or C) methylation levels in lncRNAs after inoculation, with delayed responses in Colfax compared to Williams 82. Overall, our results provide comprehensive insights into soybean responses toP. sansomeana, highlighting potential roles of lncRNAs and epigenetic regulation in plant defense.