This study investigates the role of apoptotic vesicles (apoVs) in DNA repair and cellular senescence. The authors found that apoptosis-deficient mice (both *Fas*^mut^ and *Bim*^−/−^) exhibited elevated DNA damage and premature cellular senescence, along with a significant reduction in the number of 16,000 g apoVs. Intravenous infusion of mesenchymal stromal cell (MSC)-derived 16,000 g apoVs rescued these phenotypes. Additionally, sublethal radiation exposure caused more severe DNA damage and reduced survival in *Fas*^mut^ mice compared to wild-type mice, which was also mitigated by MSC-apoV infusion. Mechanistically, the study demonstrated that apoptosis assembles multiple nuclear DNA repair enzymes, such as full-length PARP1, into 16,000 g apoVs, which are then transferred to recipient cells, leading to DNA repair and senescent cell elimination. Furthermore, embryonic stem cell-derived 16,000 g apoVs showed superior DNA repair capacity due to their higher levels of nuclear DNA repair enzymes. This study reveals a novel role for 16,000 g apoVs in safeguarding tissues from DNA damage and suggests a therapeutic strategy using stem cell-derived apoVs to ameliorate irradiation-induced DNA damage.This study investigates the role of apoptotic vesicles (apoVs) in DNA repair and cellular senescence. The authors found that apoptosis-deficient mice (both *Fas*^mut^ and *Bim*^−/−^) exhibited elevated DNA damage and premature cellular senescence, along with a significant reduction in the number of 16,000 g apoVs. Intravenous infusion of mesenchymal stromal cell (MSC)-derived 16,000 g apoVs rescued these phenotypes. Additionally, sublethal radiation exposure caused more severe DNA damage and reduced survival in *Fas*^mut^ mice compared to wild-type mice, which was also mitigated by MSC-apoV infusion. Mechanistically, the study demonstrated that apoptosis assembles multiple nuclear DNA repair enzymes, such as full-length PARP1, into 16,000 g apoVs, which are then transferred to recipient cells, leading to DNA repair and senescent cell elimination. Furthermore, embryonic stem cell-derived 16,000 g apoVs showed superior DNA repair capacity due to their higher levels of nuclear DNA repair enzymes. This study reveals a novel role for 16,000 g apoVs in safeguarding tissues from DNA damage and suggests a therapeutic strategy using stem cell-derived apoVs to ameliorate irradiation-induced DNA damage.