The clinical use of conventional medications for inflammatory bowel disease (IBD) is often limited by significant side effects. The extracellular vesicles derived from plant-based diets have shown promise in mitigating disease. Here, we discovered that natural extracellular vesicles from tea (TEVs) can achieve an appropriate transition from proinflammatory (M1) to anti-inflammatory (M2) macrophages and inhibit inflammation response both in vitro and in vivo. More importantly, the therapeutic effects of TEVs were at least partially attributed to RNA in a DSS-induced colitis model. Small RNA sequencing revealed a distinct enrichment of miRNAs in TEVs, with target genes primarily linked to IBD. TEVs were absorbed by macrophages in a time-dependent manner, carrying miRNAs that modulate gene expression within host cells. Notably, TEV-derived osa-miR166d-5p and gma-miR396a-3p were shown to enhance M2 macrophage polarization and reduce inflammation in vitro. Mechanistically, the osa-miR166d-5p- and gma-miR396a-3p-mediated targeting of the 3'-UTRs of AKT1 and IKBKB decreased NF-kappaB levels. Overall, we demonstrated that TEVs can ameliorate mouse colitis by reprogramming macrophage polarization and contain a unique miRNA repertoire, including osa-miR166d-5p and gma-miR396a-3p, with a novel function of alleviating intestinal inflammation.