Peanut (Arachis hypogaea L.) bacterial wilt (BW) is a devastating soil-borne disease caused by Ralstonia solanacearum (RS) that poses a significant threat to peanut yield and quality. Nucleotide-binding leucine-rich repeat (NBS-LRR) proteins are a class of plant-specific immune receptors that recognize pathogen-secreted effector molecules and activate immune responses to resist pathogen infections. However, the precise functions of AhCN genes (where CN is a class of nucleotide-binding site, leucine-rich repeat receptor (NLR) genes that lack LRR structural domains) in peanut plants are not fully understood. In this study, a total of 150 AhCN genes were identified and classified into nine subfamilies based on a systematic phylogenetic analysis. The AhCN genes showed highly conserved structural features, and the promoter cis-elements indicated involvement in plant hormone signaling and defense responses. After inoculation with RS, the highly resistant peanut variety ‘H108’ significantly outperformed the susceptible variety ‘H107’ based on physiological indicators such as plant height, main stem diameter, and fresh weight, likely due to the inhibition of bacterial proliferation and diffusion in the stem vascular bundle. AhCN34 was found to be significantly upregulated in ‘H108’ compared to ‘H107’ during plant infection and in response to treatments with each of three plant hormones. Importantly, AhCN34 overexpression in peanut leaves enhanced their resistance to BW. These findings demonstrate the great potential of AhCN34 for applications in peanut resistance breeding. Our identification and characterization of the AhCN genes provide insights into the mechanisms underlying BW resistance in peanut and can inform future research into genetic methods of improving BW resistance in peanut.