Mammalian genomes are extensively transcribed, which produces a large number of both coding and non-coding transcripts. Various RNAs are physically associated with chromatin, through being either retained in cis at their site of transcription or recruited in trans to other genomic regions. Driven by recent technological innovations for detecting chromatin-associated RNAs, diverse roles are being revealed for these RNAs and associated RNA-binding proteins (RBPs) in gene regulation and genome function. Such functions include locus-specific roles in gene activation and silencing, as well as emerging roles in higher-order genome organization, such as involvement in long-range enhancer-promoter interactions, transcription hubs, heterochromatin, nuclear bodies and phase transitions.