Rhizoctonia solani anastomosis group (AG) 3-PT is a devastating pathogenic fungus that causes several diseases in potatoes both in South Africa and globally. The removal of various fungicides from the market and strict regulations on the use of synthetic chemicals make disease management difficult. Therefore, alternative, environmentally safe control measures are being considered, such as the use of biological control agents (BCAs). BCAs are an attractive alternative for improving plant and soil health of economically important crops. To identify key microbial indicators of disease suppression against R. solani AG 3-PT, a greenhouse pot trial experiment was conducted using soil from a potato-growing region in KwaZulu-Natal, South Africa. High-throughput sequencing of fungal internal transcribed spacer and bacterial 16S ribosomal RNA was used to characterize the respective fungal and bacterial community composition in the soil with and without artificial inoculation with R. solani AG 3-PT. Results indicated that the pathogen caused dysbiosis in the potato soil microbiome, leading to a shift in fungal and bacterial community composition. Differentially abundant microbial taxa in R. solani AG 3-PT inoculated soils suggest a promising potential for disease-suppressive activity. Network analysis also confirmed the presence of key taxa involved in the microbial community shifts, which could support their role in the suppression of R. solani AG 3-PT. The identification of key microbial indicators against Rhizoctonia diseases can contribute to the development of environmentally sustainable potato production systems, which are particularly important considering the implementation of the European Green Deal.