Long noncoding RNAs (lncRNAs) now outnumber protein-coding genes, yet the majority remain functionally uncharacterised. We previously discovered over 800 lncRNAs at regions identified by genome-wide association studies (GWAS) for breast cancer. In this study, we performed pooled CRISPR-Cas13d RNA knockdown screens to determine which of these lncRNAs altered cell proliferation - a fundamental trait of cancer cells. We identified 43 lncRNAs whose knockdown modulated breast cell proliferation. Among them, a lncRNA named KILR, functions as a tumour suppressor that safeguards breast cells against uncontrolled proliferation. KILR is a 6.7kb, single exon, nuclear-restricted lncRNA derived from the intron of an uncharacterised isoform of the transcriptional repressor KCTD1 (KCTD1-T5). The breast cancer risk signal associated with KILR overlaps with an eQTL analysis, indicating that the risk variants may function by modulating KILR expression. Supporting these results, mRNA stability assays in heterozygous breast cell lines showed that the half-life of KILR is significantly reduced by the risk haplotype, revealing an alternative mechanism by which variants alter cancer risk. KILR pull-down followed by mass spectrometry identified RPA1, a subunit of the RPA complex required for DNA replication and repair, as one of its binding partners. Reduced KILR expression increased the available pool of RPA1, accelerating DNA replication and promoting proliferation. Conversely, KILR overexpression induced apoptosis specifically in breast cancer cells by sequestering RPA1 in nuclear foci, depleting the cancer cells of available RPA and impairing DNA replication and repair. Our study highlights lncRNAs as important mediators of breast cancer risk, emphasizing the need to annotate all noncoding transcripts in disease-relevant cell types when evaluating GWAS variants.