Interferons (IFNs) play a central role in controlling cell growth and activating anti-tumour immune responses. Through targeted RNA sequencing and CRISPR-Cas13d screening, we identified a previously uncharacterised, risk-associated long noncoding RNA (lncRNA) called BRRIAR, that boosts IFN pathway activity in estrogen receptor-positive (ER+) breast cancer. BRRIAR is transcribed from an 11 kb super-enhancer on chromosome 3p26 and is predominantly expressed in ER+ breast tumours. Functional studies revealed that BRRIAR acts both in cis and in trans. In the nucleus, BRRIAR facilitates chromatin looping to regulate BHLHE40 expression, a transcription factor involved in cytokine regulation. In the cytoplasm, BRRIAR binds RIG-I, a pattern recognition receptor critical for innate immune sensing. Rather than directly activating RIG-I, BRRIAR primes the receptor, enhancing its responsiveness to classical RIG-I ligands and promoting pro-inflammatory cytokine production. When delivered as an in vitro transcribed (IVT) RNA, BRRIAR rapidly induced dose-dependent apoptosis specifically in ER+ breast cancer cells and activated immune responses in human peripheral blood mononuclear cells. In vivo, lipid nanoparticle delivery of IVT BRRIAR triggered tumour-intrinsic IFN production, suppressed tumour growth, and extended survival in mouse models. Strikingly, IVT BRRIAR-mediated cell death was restricted to ER+ breast tumours that endogenously express BRRIAR, highlighting its dual potential as a predictive biomarker and a tumour-selective RNA therapeutic. Together, these findings reveal a novel link between genetic risk, lncRNA function, cancer immunosurveillance and breast tumourigenesis, establishing BRRIAR as a promising lncRNA-based therapeutic candidate for ER+ breast cancer.