Understanding the genetic and environmental factors that structure root-associated microbiomes is necessary to inform rice (Oryza sativa L.) breeding and fertilizer. Herein, we comprehensivly explored the microbiomes along four fine-scale root compartments, bulk soil, rhizosphere, rhizoplane and endosphere, between traditional Japonica rice and improved hybrid rice acorss three spatially distant locations. Bacterial diversity decreased monotonically from external bulk soil to internal endosphere. The acquisition of endosphere symbionts is governed conjointly by a two-step selection process and an amplification selection process, which depends on the bacterial functional group. The bacterial communities are primarly affected by root compartment and planting location, followed by relatively samll but signifcant rice genotype effect. The exterior bulk soil, rhizosphere and rhizoplane communities are govrned by variable selection. In contrast, the internal endosphere counterparts are shapped by homogenizing selection, which are undiscernible between the two rice genotypes. After ruling out planting location effect, we screened 12 rice genotype-discriminatory orders that contributed an overall 97.22 % accuracy in diagnosing rice genotype. Hybrid rice is inferior to Japonica rice in carbon and nitrogen fixation, nitrogen and phosphorus biomineralization from organic sources. Collectively, we proposed a conceptual model to infer rice genotype effect on the rhizosphere microbiomes, and the subsequent requirement of external fertilizer for sustaining yield. Our findings deepen our understanding of the complex rice genotype–root microbiomes–fertilizer interactions from the prespective of microbially-mediated nutrient cycles.