Bacterial extracellular vesicles (BEVs) are nanoscale particles secreted by microbes that serve multifunctional roles in microbial physiology and microbe-host communication. In the densely populated gastrointestinal tract, BEVs from the human commensal Bacteroides thetaiotaomicron act as high-affinity scavengers of essential micronutrients, including cobamides and iron, via specific vesicle-associated binding proteins. These BEVs not only deliver nutrients back to the parent bacterium but can sequester them from competing microbes, supporting survival in nutrient-limited environments. Beyond microbial nutrition, BEVs traverse host barriers to deliver bioactive cargo systemically. Using a highly sensitive NanoLuciferase-based tracking system in germ-free and conventional mice, we demonstrate that naturally produced BEVs cross the intestinal epithelium and vascular endothelium, reaching distal tissues including the brain and eyes. Functional assays show that proteins carried by BEVs remain active upon host delivery, revealing a covert pathway by which gut bacteria influence host physiology without direct epithelial contact. Together, these findings establish BEVs as versatile “nanoscale multitools” that integrate nutrient acquisition and long-range molecular delivery, highlighting their dual role in microbial ecology and host communication. Understanding the mechanisms governing BEV cargo selection, barrier traversal, and tissue targeting provides a foundation for exploiting these vesicles as novel therapeutic delivery systems and for deciphering microbiota-host interactions at the molecular level.