We provide a portrait of the bacterial transcription apparatus in light of the data emerging from structural studies, sequence analysis and comparative genomics to bring out important but underappreciated features. We first describe the key structural highlights and evolutionary implications emerging from comparison of the cellular RNA polymerase subunits with the RNA-dependent RNA polymerase involved in RNAi in eukaryotes and their homologs from newly identified bacteria: selfish elements. We describe some previously unnoticed domains and the possible evolutionary stages leading to the RNA polymerases of extant life forms. We then present the case for the ancient orthology of the basal transcription factors, the sigma factor and TFIIB, in the bacterial and the archaeo-eukaryotic lineages. We also present a synopsis of the structural and architectural taxonomy of specific transcription factor; and their genome-scale demography. In this context, we present certain notable deviations from the otherwise invariant proteome-wide trends in transcription factor distribution and use it to predict the presence of an unusual lineage-specifically expanded signaling system in certain firmicutes like Paenibacillus. We then discuss the intersection between functional properties of transcription factors and the organization of transcriptional networks. Finally, we present some of the interesting evolutionary conundrums posed by our newly gained understanding of the bacterial transcription apparatus and potential areas for future explorations. Published by Elsevier Inc.