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Regular application of mineral and organic fertilizers is one of the essential components of agricultural intensification. The application of fertilizers leads to the artificial enrichment of the soil with readily available substrates and biophilic elements, which can have a significant impact on the soil and rhizosphere microbiome. We studied the impact of different fertilizer systems on the quantitative parameters of various microbial groups in a soddy-podzolic soil (Umbric Albic Retisol) and the rhizosphere of potatoes and barley. The study was carried out on a long-term field experiment, in which mineral (NPK), organic (manure), and mixed (NPK + manure) fertilizer systems had been applied since 1968. The application of organic fertilizers increased the microbial biomass carbon (Cmic) in the bulk soil and the rhizosphere by 25–100% compared to the soil without fertilizers, while the use of mineral fertilizers, on the contrary, decreased the microbial biomass by 10–30%. Basal respiration and metabolic quotient (qСО2) increased in the following order: without fertilizers < NPK < NPK + manure < manure. The gene copy numbers of bacteria, archaea, and fungi significantly increased (by 1.5–2.5 times) under organic fertilizers and decreased (2–2.5 times) under NPK. The fungi/bacteria ratios varied from 32 to 100 and from 0.10 to 0.92 according to luminescent microscopy and quantitative PCR methods, respectively. The lowest ratios were revealed for variants with NPK, and the highest fungi/bacteria ratios were in variants with manure. Thus, the applied doses of mineral fertilizers should be compensated by the addition of fresh organic matter in order to maintain the stability of the soil—microorganisms—plant system. [ABSTRACT FROM AUTHOR]