The root-knot nematode (RKN) disease is a highly destructive soilborne disease that significantly affects peanut yield in Northern China. The composition of the soil microbiome plays a crucial role in plant disease resistance, particularly for soilborne diseases like RKN. However, the relationship between the occurrence of RKN disease and the structure and diversity of bacterial communities in peanut fields remains unclear. To investigate bacterial diversity and the community structure of peanut fields with severe RKN disease, we applied 16S full-length amplicon sequencing based on the third high-throughput sequencing technology. The results indicated no significant differences in soil bacterial α-diversity between resistant and susceptible plants at the same site. However, the Simpson index of resistant plants was higher at the site of peanut-wheat-maize rotation (Ro) than that at the site of peanut continuous cropping (Mo), showing an increase of 21.92%. The dominant phyla identified in the peanut bulk soil included Proteobacteria, Acidobacteria, Actinobacteria, Planctomycetes, Chloroflexi, Firmicutes, and Bacteroidetes. Further analysis using LEfSe (Linear discriminant analysis effect size) revealed that Sulfuricellaceae at the family level was a biomarker in the bulk soil of susceptible peanut compared to resistant peanut. Additionally, Singulisphaera at the genus level was significantly more enriched in the bulk soil of resistant peanut than that of susceptible peanut. Soil properties were found to contribute to the abundance of bacterial operational taxonomic units (OTUs). Available phosphorus (AP), available nitrogen (AN), organic matter (OM), and pH made a positive contribution to the bacterial OTUs, while available potassium (AK) made a negative contribution. The metabolic pathway of novobiocin biosynthesis was only enriched in soil samples from resistant peanut plants. Eleven candidate beneficial bacteria and ten candidate harmful strains were identified in resistant and susceptible peanut, respectively. The identification of these beneficial bacteria provides a resource for potential biocontrol agents that can help improve peanut resistance to RKN disease. Overall, the study demonstrated that severe RKN disease could reduce the abundance and diversity of bacterial communities in peanut bulk soil. The identification of beneficial bacteria associated with resistant peanut offered the possibility for developing biocontrol strategies to enhance peanut resistance to RKN disease.