Heterochromatic repetitive satellite RNAs are extensively transcribed in a variety of human cancers, including BRCA1 mutant breast cancer. Aberrant expression of satellite RNAs in cultured cells induces the DNA damage response, activates cell cycle checkpoints, and causes defects in chromosome segregation. However, the mechanism by which satellite RNA expression leads to genomic instability is not well understood. Here we provide evidence that increased levels of satellite RNAs in mammary glands induce tumor formation in mice. Using mass spectrometry, we further show that genomic instability induced by satellite RNAs occurs through interactions with BRCA1-associated protein networks required for the stabilization of DNA replication forks. Additionally, de-stabilized replication forks likely promote the formation of RNA-DNA hybrids in cells expressing satellite RNAs. These studies lay the foundation for developing novel therapeutic strategies that block the effects of non-coding satellite RNAs in cancer cells. Display omitted •Satellite RNAs induce DNA damage•Elevated satellite transcripts induce tumor formation•Satellite RNAs bind to the BRCA1 protein complex•Increased levels of satellite RNAs destabilize DNA replication forks Heterochromatin-encoded satellite RNAs are often aberrantly expressed in human cancers. Zhu et al. show that these RNAs can promote breast cancer formation and that they bind BRCA1 and associated proteins that are important for replication fork stability and genomic instability.