In DNA repair, the resection of double-strand breaks dictates the choice between homology-directed repair-which requires a 3' overhang-and classical non-homologous end joining, which can join unresected ends(1,2). BRCAl-mutant cancers show minimal resection of double-strand breaks, which renders them deficient in homology-directed repair and sensitive to inhibitors of poly(ADP-ribose) polymerase 1 (PARP1)(3-8). When BRCA1 is absent, the resection of double-strand breaks is thought to be prevented by 53BP1, RIF1 and the REV7-SHLD1-SHLD2-SHLD3 (shieldin) complex, and loss of these factors diminishes sensitivity to PARP1 inhibitors(4,6-9). Here we address the mechanism by which 53BP1-RIF1-shieldin regulates the generation of recombinogenic 3' overhangs. We report that CTC1-STN1-TEN1 (CST)(10), a complex similar to replication protein A that functions as an accessory factor of polymerase-alpha (Pol alpha)-primase(11), is a downstream effector in the 53BP1 pathway. CST interacts with shieldin and localizes with Pol alpha to sites of DNA damage in a 53BP1- and shieldin-dependent manner. As with loss of 53BP1, RIF1 or shieldin, the depletion of CST leads to increased resection. In BRCA1-deficient cells, CST blocks RAD51 loading and promotes the efficacy of PARP1 inhibitors. In addition, Pol alpha inhibition diminishes the effect of PARP1 inhibitors. These data suggest that CST-Pol alpha-mediated fill-in helps to control the repair of double-strand breaks by 53BP1, RIF1 and shieldin.