Budding yeast cells suffering a single, unrepaired DNA double strand break (DSB) arrest prior to anaphase for 12–15 h, in a Mec1 (ATR)‐dependent manner, following which checkpoint signaling is down‐regulated to allow resumption of cell cycle progression in a phenomenon known as adaptation. A similar, but not genetically equivalent process of recovery occurs after the DSB has been repaired. In this study, we found that inducing autophagy in wild‐type cells suffering DNA damage, either by the addition of rapamycin, by overexpression of a dominant‐active version of Atg13 (ATG13–8SA) or by deletion of genes required for Golgi‐Associated Retrograde Transport (GARP) prevented both adaptation and recovery. These effects were due to the DNA damage‐dependent mislocalization of the mitotic activator Esp1 (Separase) via the degradation of its chaperone/inhibitor Pds1 (Securin). Failure to adapt is dependent on vacuolar proteases and autophagy, as these defects were suppressed by 1) deleting the vacuolar protease genes or by 2) deleting Autophagy related genes (specifically those required for the Cytoplasm‐to‐Vacuole transport (CVT) pathway). Overexpression of ATG13–8SA also promoted the mislocalization of Pds1 and Esp1 after induction of a DSB. Arrest persisted even as Rad53 (Chk2) hyperphosphorylation diminished after 12–15 h. Finally we note that ATG13–8SA overexpressing cells were sensitive to a wide‐array of DNA damaging agents and autophagy mutants displayed a reduced duration of checkpoint arrest. Overall, our results suggest a role for DNA damage‐induced autophagy in maintaining robust checkpoint arrest by targeting mitotic activators for degradation and specifically implicate the CVT pathway as a target of the DNA damage checkpoint.