DNA polymerase epsilon (Polε) carries out leading strand synthesis with high fidelity owing to its exonuclease activity. Polε polymerase and exonuclease activities are in balance, due to partitioning of nascent strands between catalytic sites, so that net end resection occurs when synthesis is impaired. Stalling of chromosomal DNA synthesis activates replication checkpoint kinases, required to preserve the functional integrity of replication forks. We found that Polε is phosphorylated in a Rad53CHK1-dependent manner upon fork stalling, likely to limit Polε-driven nascent strand resection that causes replication fork collapse. In stress conditions Polε phosphorylation occurs on serine 430 of the Pol2 catalytic subunit. A S430 phosphomimic limits strand partitioning and exonucleolytic processivity, while non-phosphorylatable Pol2-S430A bypasses checkpoint regulation causing stalled fork resection and collapse. We propose that checkpoint kinases switch Polε to an exonuclease-safe mode by curbing active site partitioning thus preventing nascent strand resection and stabilizing stalled replication forks. 