Plant root activities lead to significant differences in metabolites between the rhizosphere and non-rhizosphere soil, profoundly affecting microbial distribution. However, how this process drives the migration and propagation of manure-derived antibiotic resistance genes (ARGs) in farmland ecosystems remains unclear. Herein, we used a rice pot microcosm experiment to explore the characteristics of antibiotic resistome and bacterial communities in rhizosphere and non-rhizosphere soils and the driving effects of rhizosphere metabolites on ARG propagation. The results showed significant differences in some ARGs and bacterial diversity in rhizosphere and non-rhizosphere soils with varied differential ARGs between different growth stages of rice (P < 0.05). The biosynthesis of secondary metabolites and glutathione metabolism were found to be the main pathways affecting ARG differences in rhizosphere and non-rhizosphere soils under manure application. Structural equation modeling (SEM) analysis further indicated that ARG distribution differences between rhizosphere and non-rhizosphere soils were mainly regulated by differential metabolites, which influenced the ARG distribution by altering the succession of soil microbial communities. These results demonstrate the role of differential metabolites resulting from rice root activities in co-regulating ARG distribution, providing new insights into the regulatory mechanisms of soil ARG dynamics in paddy fields.