Transcription is the first step of gene expression, which is carried out by DNA-dependent RNA polymerases. RNA polymerases are considered to be well-regulated molecular machines that immediately initiate a new round of transcription after having been released from DNA and RNA during termination. However, RNA polymerases can become trapped in unproductive binary complexes with DNA or RNA. Polymerases trapped in this form endanger genome stability and lead to reduced pools of free polymerase. Moreover, RNA polymerases can enter dormant states. Recycling factors help retrieve RNA polymerases from trapped states, but their mechanisms remain elusive. Here we analyzed complexes of Bacillus subtilis RNA polymerase bound to a recycling ATPase, HelD, by cryo-electron microscopy, crosslinking / mass spectrometry and structure-informed biochemical analyses. HelD exhibits UvrD-like helicase domains from which a Gre-cleavage factor-like coiled-coil and a unique helical protrusion extend like two prongs. The coiled-coil inserts deep into the secondary channel of RNA polymerase, rearranges the active center and competes with bound RNA. The helical protrusion inserts into the primary channel, pushing the β and β' subunits apart and competing with downstream DNA. Insertion of the protrusion into the primary channel is aided by the intrinsically unstructured C-terminal region of the RNA polymerase δ subunit. The recovery of the polymerase is completed by ATP-mediated HelD release. We additionally observed a dimeric RNA polymerase-HelD complex, which suggests that HelD can also induce a dormant state at low ATP levels. Our results explain how HelD in collaboration with the δ subunit can rescue RNA polymerase entrapped on virtually any nucleic acid and suggest that HelD regulates transcriptional activity depending on the nutritional status of the cell.