The temperate bacteriophage 186, after infecting its host bacterium Escherichia coli, makes a simple developmental decision, directing resources to either the lytic or the lysogenic developmental pathways. Crucial to this decision is the CII protein. This potent transcriptional factor activates the early lysogenic promoter pE at least 400-fold, to build up sufficient immunity repressor levels so that a significant fraction of infections commit to lysogeny. Its potency and its unusual property of binding to operator sites separated by 20 base pairs, center-to-center, suggests it may activate the pE promoter by a novel mechanism. Three crystal structures of the CII protein were solved to 2-3Å. The structures reveal a tetrameric arrangement of CII, shown to be necessary for DNA binding by mutational analysis and native mass-spectrometry. CII is degraded in vivo by both RseP and FtsH to give a transcriptionally inactive product, suggesting CII may act as a sensor of host metabolic activity. The crystal structures reveal a reduced self-association of the degradation product and explain the loss of activity. Modelling of the CII-RNA polymerase complex at the pE promoter suggests that CII activates pE via recruitment of RNA polymerase through both σ70 and α-CTD contacts, in an arrangement different to previously studied transcriptional activators.