Dynamic covalent chemistry (DCC) offers a powerful strategy for directing molecular assembly through reversible bond formation under thermodynamic control. Here, we extend this concept to RNA by exploiting the formation of 2′,3′-cyclic phosphates during cleavage, enabling the re-ligation of RNA strands into defined structures catalysed by RNase T1. This approach allows for the sequence-selective assembly of folded RNA hairpins from short fragments, without the need for chemical activation or high-energy cofactors such as ATP. Hairpin formation proceeds with high specificity even in complex mixtures, reaching yields of up to 49% under aqueous conditions. Thermodynamic modelling reveals loop sequence and size as a key determinant of ligation efficiency, and yields can be further enhanced through the addition of hairpin-binding peptides. Not only might RNA DCC have contributed to the emergence of the first genomes during the origin of life, it also offers promising new avenues for synthetic RNA technologies, including the modular construction of guide RNAs for CRISPR–Cas systems.