Iron (Fe) is an essential nutrient for most bacterial pathogens. In these organisms, a variety of regulatory systems that respond to specific Fe complexes found within their vertebrate hosts have evolved. In Bordetella avium, the heme utilization locus encoded by rhuIR-bhuRSTUV mediates efficient acquisition of Fe from heme and hemoproteins. Control of bhuRSTUV expression is promulgated at two levels. When Fe is abundant, expression is repressed in a Fur-dependent manner which is partially relieved when Fe is limiting. In the presence of heme or hemoproteins, expression of the bhuRSTUV operon is induced via a three-component signal transduction cascade composed of RhuI, RhuR, and BhuR. Herein, we report the identification of two promoters (PrhuI and PbhuR) that control expression of the rhuIR-bhuRSTUV cluster. Primer extension analysis identified the transcriptional start site of PrhuI within a putative Fur box. Transcriptional initiation of PbhuR mapped within the rhuR-bhuR intergenic region. Maximal transcription from PbhuR required Fe-limiting conditions, the presence of heme (or hemoglobin), and rhuI; however, analysis of transcripts produced from the rhuIR-bhuRSTUV locus revealed a pattern of low-level bhuR transcription in the absence of heme which originated from both PbhuR and PrhuI. Transcription from PrhuI was repressed by Fe in the presence of fur and somewhat enhanced by the addition of hemin to Fe-limited media. The nature of this hemin-associated PrhuI stimulation was rhuI independent and therefore not induced by heme via the BhuR-RhuR-RhuI signal cascade. Fe also repressed transcription from PbhuR in a fur-dependent manner; however, activation from this promoter, in the presence or absence of heme, did not occur without rhuI.