BRCA1/2-deficient cancers are hypersensitive to genotoxic agents and toxicity has traditionally been attributed to the inability to repair or prevent DNA double stranded breaks (DSBs). Here, we attribute the toxicity to an inability to protect single stranded DNA (ssDNA) replication gaps. We re-asses the roles of canonical DSB damage responders 53BP1-MDC1-H2AX and investigate their role in unperturbed conditions during replication. MDC1, like 53BP1, is enriched in the chromatin of BRCA1-deficient cells. Its loss, like 53BP1, confers resistance to poly (ADP)-ribose polymerase (PARP) inhibitors and translesion synthesis (TLS) inhibitors by gap suppression and reducing PARP1 activity. In BRCA1-deficient cells, RAD51 fails to form nuclear “foci” in response to DNA damage, supporting a model that PARPi sensitivity is due to a loss of RAD51 function in homologous recombination (HR). 53BP1 loss, which counteracts HR by blocking end resection, enhances PARPi resistance and recovers RAD51 foci, further linking these outcomes. Unexpectantly, we find that RAD51 is essential and enriched in the chromatin of BRCA1-deficient cells, while deletion of 53BP1 alleviates this enrichment and dependency. The same pattern evolves along with PARPi resistance following loss of MDC1 or H2AX. We link these factors to 53BP1 nuclear bodies associated with ssDNA gaps in BRCA1-deficient cells. Unlike 53BP1 loss however, loss of MDC1 and H2AX in BRCA1 deficient cells does not restore RAD51 foci, further uncoupling HR from PARPi resistance. Collectively, we propose a model that gaps necessitate RAD51 chromatin enrichment for cell survival which limits its availability for other functions and reveals a targetable dependency.