DNA double-strand breaks (DSBs) are cytotoxic lesions that must be accurately repaired to maintain genome stability. Replication protein A (RPA) plays an important role in homology-dependent repair of DSBs by protecting the single-stranded DNA (ssDNA) intermediates formed by end resection and by facilitating Rad51 loading. We found that hypomorphic mutants of RFA1 that support intra-chromosomal homologous recombination are profoundly defective for repair processes involving long tracts of DNA synthesis, in particular break-induced replication (BIR). The BIR defects of the rfa1 mutants could be partially suppressed by eliminating the Sgs1-Dna2 resection pathway, suggesting that Dna2 nuclease attacks the ssDNA formed during end resection when not fully protected by RPA. Overexpression of Rad51 was also found to suppress the rfa1 BIR defects. We suggest that Rad51 binding to the ssDNA formed by excessive end resection and during D-loop migration can partially compensate for dysfunctional RPA. Display omitted •Partial destabilization of RPA binding to ssDNA modestly decreases break repair•Stable RPA-ssDNA interaction is critical for break-induced replication and gap repair•The rfa1 BIR defect is suppressed by elimination of Sgs1-Dna2 catalyzed end resection•Rad51 overexpression suppresses the rfa1 BIR defect RPA plays an important role during homology-dependent repair (HDR) to protect fragile single-stranded DNA (ssDNA) intermediates. Here, Ruff et al. show that partial destabilization of RPA binding to ssDNA has modest effects on efficient intra-chromosomal HDR reactions but causes profound defects in HDR events that involve long-lived ssDNA intermediates, such as break-induced replication (BIR). The BIR defect caused by dysfunctional RPA can be partially overcome by preventing excessive end resection or by Rad51 overexpression.