Precise regulation of the duration and extent of inflammation is crucial for balancing pathogen elimination and preventing tissue damage. The mechanisms underlying inflammation resolution are not yet fully understood. Here, we reveal that neutrophils, typically known for their pro-inflammatory role and pathogen clearance capabilities, can paradoxically aid in resolving inflammation by actively producing anti-inflammatory vesicles. Large aging neutrophil-derived vesicles (LAND-Vs) emerged in inflamed lungs during bacterial pneumonia. These vesicles, protected from efferocytotic clearance by phagocytes due to surface CD47, CD24, or CD31, accumulated in the resolution phase of inflammation and persisted at the site long after neutrophil recruitment subsided. CD55 on LAND-Vs exerted a robust, sustained anti-inflammatory effect by inhibiting complement 3 convertase and suppressing complement activity, thereby reducing neutrophil recruitment and tissue damage. A combination of neutrophil-specific CD55 knockout and adoptive transfer experiments demonstrated that LANDs were not only essential but also sufficient for efficient inflammation resolution. CD55+ LAND-Vs originated in lipid rafts, where CD55 accumulated asymmetrically during neutrophil aging, and subsequently formed through RhoA-dependent budding. Intriguingly, the number of CD55+ LAND-Vs in the peripheral blood of severe COVID-19 patients was markedly lower than that in healthy individuals or patients with milder cases of COVID-19, indicating that LAND-Vs might contribute to mitigating pathologies observed in severe COVID-19 patients. In conclusion, LAND-Vs, a unique structure originating from aging neutrophils, emerges as a pivotal physiological immunomodulator and showcases functions that transcend the limited lifespan of neutrophils, offering a promising therapeutic target for inflammatory and infectious diseases.