DNA double-strand breaks (DSBs) accumulate in mitosis in response to DNA replication stress or deficiency in breast cancer susceptibility type 1 and 2 (BRCA1/2). This is a critical threat to genome stability as the classical DSB repair pathways non-homologous end joining (NHEJ) and homologous recombination (HR) are repressed(1-7). Instead, mitotic repair relies on the processes of microhomology-mediated end joining (MMEJ) or mitotic DNA synthesis (MiDAS), but how these pathways are coordinated and regulated remains unclear.  Here, we reveal that the CIP2A-TOPBP1 axis orchestrates DSB repair in mitosis by promoting CDK1-driven phosphorylation of SLX4 at Thr1260, recruiting the SMX complex to promote MiDAS. In addition, the CIP2A-TOPBP1 axis regulates mitotic Polθ recruitment and MMEJ. This dual mechanism ensures coordinated DSBs repair by integrating spatial control of TOPBP1-CIP2A chromatin recruitment with the temporal regulation provided by mitotic kinases, thereby preserving genome stability. These findings provide new insights into DSB repair dynamics in mitosis and offer a mechanistic rationale for the synthetic lethality of CIP2A in BRCA1/2-deficient tumors through the simultaneous impairment of break induced replication (BIR)-like MiDAS and MMEJ, which are genetically redundant pathways to HR.