ZNF827 is a C2H2 zinc finger protein that was initially identified to function in concert with the nucleosome remodelling and deacetylase complex to remodel telomeric chromatin and promote homologous recombination at telomeres. Using a combination of biochemistry, and cell and molecular biology techniques, including protein purification, electrophoretic mobility shift assays, co-immunoprecipitation, flow cytometry, and fixed and live cell microscopy, we have identified ZNF827 as a novel single-stranded (ss) DNA binding protein involved in the DNA damage response. Specifically, we found that ZNF827 displays preferential binding to ssDNA in a non-sequence specific manner. We further demonstrated that ZNF827 directly interacts with the major human ssDNA binding protein RPA. Removal of DNA by benzonase disrupted the RPA-ZNF827 interaction, suggesting that ZNF827 interacts with RPA in its ssDNA-bound state. Upon replication stress and replication-associated DNA damage induction, ZNF827 colocalised with γH2AX and replication forks marked by PCNA, suggesting that ZNF827 functions at stalled forks. ZNF827 depletion dampened S345 phosphorylation of CHK1 and S33 phosphorylation of RPA2, both downstream effectors of ATR signalling. Homologous recombination (HR) was reduced following ZNF827 depletion, as evidenced by a reduction in sister chromatid exchange events and HR reporting events. Collectively, these results support a role for ZNF827 as a novel player in the ATR-mediated DNA damage response and homology-directed repair.