This study identifies a new way to maintain telomere integrity involving nucleostemin. Loss of nucleostemin increased the formation of telomere damage foci, and in telomerase-inactive cells (which instead use alternative lengthening of telomeres (ALT)), it decreased the number of ALT-associated PML bodies (APBs; which may have a role in damage repair by homologous recombination (HR)) and the percentage of telomeres associated with APBs. So how does nucleostemin protect telomeres? In ALT cells, nucleostemin increased the sumoylation of the telomere protein TRF1 (which is required for APB formation) and promoted its association with the PML body protein PML-IV. Furthermore, the sumoylated TRF1–PML-IV interaction was induced following DNA damage in a nucleostemin-dependent manner, and this was required for the recruitment of the HR protein RAD51 to damage sites. Importantly, this mechanism was conserved in telomerase-active cells.