Most haplotype blocks linked to human complex traits and disorders by genome-wide association studies (GWAS) lack protein-coding sequences and are presumed to harbor DNA regulatory variants. Many GWAS regions overlap enhancer elements and most express long noncoding RNAs (lncRNAs). Here we mapped long noncoding RNAs expressed from breast cancer GWAS regions and identify 876 that are linked to breast cancer risk. CRISPR-Cas13d knockdown screens for 2D, 3D and in vivo proliferation identified several lncRNAs whose knockdown alter breast cancer proliferation. We show that one of these lncRNAs, KILR, acts as a tumor suppressor, safeguarding breast cells against uncontrolled proliferation. The half-life of KILR is significantly reduced in the presence of the risk haplotype, revealing an alternative mechanism by which genetic variants at GWAS loci alter disease risk. Mechanistically, KILR sequesters RPA1, a subunit of the RPA complex required for DNA replication and repair. Reduced KILR expression promotes breast cancer cell proliferation by increasing the available pool of RPA1 and speed of DNA replication. Conversely, KILR overexpression promotes apoptosis in breast cancer cells, but not normal breast cells. These findings confirm lncRNAs as mediators of breast cancer risk, emphasize the need to annotate noncoding transcripts in relevant cell types when investigating GWAS variants and provide a scalable platform for mapping phenotypes associated with lncRNAs.