ABSTRACT Bacterial wilt (BW) is a devastating disease caused by Ralstonia solanacearum , which leads to severe yield and quality losses in peanuts ( Arachis hypogaea L.). Though pathogenesis‐related ( PRs ) genes are crucial for plants to cope with various diseases, the research on peanut PR superfamily genes ( AhPRs ) is limited. Herein, genome‐wide identification revealed 883 AhPR genes belonging to 16 subfamilies ( AhPR1 ‐ AhPR12 , AhPR14 ‐ AhPR18 ). Gene ontology (GO) analysis and weighted gene co‐expression network analysis (WGCNA) indicated that 135 core AhPRs are associated with the peanut resistance to BW at both seedling and flowering stages. Additionally, 49 key AhPRs significantly up‐regulated in H108 (BW‐resistant cultivar) but not in H107 (BW‐sensitive cultivar) in response to BW infection were screened out for further phylogenetic analysis. Expression analysis of 15 AhPRs having a close relationship with reported disease‐resistant‐related PR homologous genes suggested that AhPR10‐54 plays key roles in peanut resistance against BW and in response to phytohormone induction. Subcellular localization analysis revealed that the fusion protein AhPR10‐54‐YFP is specifically expressed in the nucleus and on the plasma membrane. Furthermore, transient overexpression of AhPR10‐54 triggers hypersensitive response (HR) and enhances the resistance against R. solanacearum in tobacco leaves. Our findings not only expanded the understanding of PR10 in plant defense responses but also provided novel insights into peanut resistance against BW.