Recognition of promoters in bacterial RNA polymerases (RNAPs) is controlled by their sigma subunits that first bind to a double-stranded DNA element ~35 to ~14 nucleotides upstream of the transcription start site (TSS) and then capture several bases of the non-template strand ~10 nucleotides upstream of the TSS. Here, we shift this paradigm and explain the mechanism by which the phage AR9 non-virion RNAP (nvRNAP), a bacterial RNAP homolog, recognizes a −10 promoter element in the template strand directly. Together, the AR9 nvRNAP sigma-like subunit, the enzyme core, and the template strand itself form two nucleotide base-accepting pockets whose shapes dictate the AR9 nvRNAP’s deoxyuridine promoter requirement. A single amino acid substitution in the promoter specificity subunit allows one of these pockets to accept a thymine base thus expanding the enzyme’s promoter consensus. Our work demonstrates the extent to which viruses can evolve host-derived multisubunit enzymes to control host takeover.