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Abstract Background Rice cultivation relies on planting grains harboring beneficial microbiota. However, the origination, distribution, and transmission dynamics of grain-borne bacteria remain unclear. Results Using rice grain as a model system, this study investigates the primary sources, major niches in seeds, and the dynamics of community acquisition, maintenance, and transmission between generations of grain-borne bacteria. Quantitative PCR and 16S rRNA gene sequencing demonstrate rice grains acquiring bacteria primarily from the external environment during panicle heading and flowering. These bacteria concentrate between the caryopsis and glumes, establishing sizable communities in developing seeds. The dominant taxa included Pantoea, Pseudomonas, and Sphingomonas. Throughout seed development and storage, community structure remains consistent while abundance fluctuates within one order of magnitude. Upon germination under axenic conditions, seed bacteria successfully colonize shoots and roots of offspring seedlings. However, bacteria transmitted solely through internal routes fail to form comparably large communities. Analysis of taxonomic composition uncovers dramatic reshaping from seeds to seedlings, potentially reflecting functional adaptation. Conclusions We clarify seed-borne bacterial origination, acquisition timing, seed colonization, intergenerational transmission, and seedling diversification. Our findings provide novel insights into rice seed bacterial dynamics critical for microbiome management. Video Abstract