As one of the most important and largest transcription factors, WRKY plays a critical role in plant disease resistance. However, little is known regarding the functions of the WRKY family in cultivated peanuts (Arachis hypogaea L.). In this study, a total of 174 WRKY genes (AhWRKY) were identified from the genome of cultivated peanuts. Phylogenetic analysis revealed that AhWRKY proteins could be divided into four groups, including 35 (20.12%) in group I, 107 (61.49%) in group II, 31 (17.82%) in group III, and 1 (0.57%) in group IV. This division is further supported by the conserved motif compositions and intron/exon structures. All AhWRKY genes were unevenly located on all 20 chromosomes, among which 132 pairs of fragment duplication and seven pairs of tandem duplications existed. Eighteen miRNAs were found to be targeting 50 AhWRKY genes. Most AhWRKY genes from some groups showed tissue-specific expression. AhWRKY46, AhWRKY94, AhWRKY156, AhWRKY68, AhWRKY41, AhWRKY128, AhWRKY104, AhWRKY19, AhWRKY62, AhWRKY155, AhWRKY170, AhWRKY78, AhWRKY34, AhWRKY12, AhWRKY95, and AhWRKY76 were upregulated in ganhua18 and kainong313 genotypes after Ralstonia solanacearum infection. Ten AhWRKY genes (AhWRKY34, AhWRKY76, AhWRKY78, AhWRKY120, AhWRKY153, AhWRKY155, AhWRKY159, AhWRKY160, AhWRKY161, and AhWRKY162) from group III displayed different expression patterns in R. solanacearum sensitive and resistant peanut genotypes infected with the R. solanacearum. Two AhWRKY genes (AhWRKY76 and AhWRKY77) from group III obtained the LRR domain. AhWRKY77 downregulated in both genotypes; AhWRKY76 showed lower-higher expression in ganhua18 and higher expression in kainong313. Both AhWRKY76 and AhWRKY77 are targeted by ahy-miR3512, which may have an important function in peanut disease resistance. This study identified candidate WRKY genes with possible roles in peanut resistance against R. solanacearum infection. These findings not only contribute to our understanding of the novel role of WRKY family genes but also provide valuable information for disease resistance in A. hypogaea.