RNA folding in the cell occurs during transcription. Expedient RNA folding must avoid the formation of undesirable structures as the nascent RNA emerges from the RNA polymerase. We show that efficient folding during transcription of three conserved non-coding RNAs from E. coli, RNase P RNA, SRP RNA and tmRNA is facilitated by their cognate polymerase pausing at specific locations. These pause sites are located between the upstream and the downstream portions of all the native long-range helices in these non-coding RNAs. In the paused complexes, the nascent RNAs form labile structures that sequester these upstream portions in a manner as to guide folding. Both the pause sites and the secondary structure of the non-native portions of the paused complexes are phylogenetically conserved. Specific pausing-induced structural formation can be a general strategy to facilitate the folding of long-range helices. This polymerase-based mechanism may result in portions of non-coding RNA sequences to be evolutionarily conserved for efficient folding during transcription.