PARP inhibitors (PARPi), either as monotherapy or in combination with chemotherapy, have been shown to improve progression-free survival for patients with homologous recombination (HR)-deficient triple-negative breast cancer (TNBC). However, PARPi monotherapy shows limited effectiveness in HR-proficient tumours, and acquired resistance to PARPi frequently develops. Emerging evidence has highlighted the critical roles of long noncoding RNAs (lncRNAs) in modulating the DNA damage response. In this study, we performed pooled CRISPR/Cas13 RNA screens to identify lncRNAs that play key roles in DNA repair pathways in TNBC. Our screens identified POLR2J4, an annotated but functionally uncharacterized lncRNA, as one of the top hits. POLR2J4 is a nuclear lncRNA with high expression levels in various breast cancer cell lines. CRISPR/Cas13-mediated knockdown of POLR2J4 showed a strong synergistic effect with the PARPi olaparib, improving its efficacy in both HR-deficient and HR-proficient TNBC cells. Furthermore, antisense oligonucleotide (ASO)-mediated knockdown of POLR2J4 significantly enhanced PARPi sensitivity, reducing olaparib IC50 values by three-fold in POLR2J4-ASO cells compared to parental cells. RNAseq analysis on POLR2J4-ASOs cells identified BRCA1 – a key HR repair gene – as one of the most significantly downregulated targets following POLR2J4 knockdown. Additionally, POLR2J4 knockdown combined with irradiation, markedly reduced Rad51 foci formation, indicating compromised HR repair function. Mechanistically, reduced POLR2J4 levels were shown to downregulate BRCA1 promotor activity and expression, thereby impairing HR repair and improving PARPi efficacy in HR-proficient TNBCs. These findings provide a promising RNA-based strategy to boost PARPi sensitivity in HR-proficient TNBC.