In bacteria, a primary σ-factor associates with the core RNA polymerase (RNAP) to control most transcription initiation, while alternative σ-factors are used to coordinate expression of additional regulons in response to environmental conditions. Many alternative σ-factors are negatively regulated by anti–σ-factors. In Escherichia coli, Salmonella enterica, and many other γ-proteobacteria, the transcription factor Crl positively regulates the alternative σ^S-regulon by promoting the association of σ^S with RNAP without interacting with promoter DNA. The molecular mechanism for Crl activity is unknown. Here, we determined a single-particle cryo-electron microscopy structure of Crl-σ^S-RNAP in an open promoter complex with a σ^S-regulon promoter. In addition to previously predicted interactions between Crl and domain 2 of σ^S (σ^S₂), the structure, along with p-benzoylphenylalanine cross-linking, reveals that Crl interacts with a structural element of the RNAP β′-subunit that we call the β′-clamp-toe (β′CT). Deletion of the β′CT decreases activation by Crl without affecting basal transcription, highlighting the functional importance of the Crl-β′CT interaction. We conclude that Crl activates σ^S-dependent transcription in part through stabilizing σ^S-RNAP by tethering σ^S₂ and the β′CT. We propose that Crl, and other transcription activators that may use similar mechanisms, be designated σ-activators.