Included in the genus Bordetella, are the closely related respiratory pathogens B. pertussis, B. parapertussis_hu, and B. bronchiseptica. B. pertussis and B. parapertussis_hu infection is limited to humans, with both species causing the acute respiratory disease whooping cough. Despite widespread vaccine use, reported cases of whooping cough have been on the rise over the last decade, suggesting that current vaccines do not confer lasting immunity. B. bronchiseptica infects a wide range of non-human animals, and is epidemic among animal boarding and breeding facilities. New insight into the pathogenesis of these organisms is critical for future vaccine development and disease control. Virulence gene expression in the bordetellae is regulated by the BvgAS phosphorelay, which coordinates the expression of three distinct phenotypic phases, the virulent Bvg⁺ phase, the avirulent Bvg⁻ phase, and the Bvgⁱ phase, which has been hypothesized to function in aerosol transmission. Work in chapter 2 of this dissertation characterizes BvgA∼P binding at the promoter of the Bvgⁱ phase specific gene bipA. BvgA∼P binding at the bipA promoter was shown to both activate and repress transcription. Like many phosphorelays, bvgAS expression is autoregulated. Chapter 3 of this dissertation evaluates the contribution of autoregulation on the expression of multiple phenotypic phases in response to temporal and steady-state environmental cues. Autoregulation was not necessary for proper steady-state gene regulation, but was essential for the expression of multiple phenotypic phases in response to a shift from Bvg⁻ phase conditions to Bvg⁺ phase conditions. Even though host specificity and disease severity conferred by B. pertussis and B. parapertussis _hu are different than in B. bronchiseptica, these species are very closely related, and it is widely acknowledged that they should be considered subspecies. Despite genome comparison, the underlying basis of host specificity and disease between these organisms is unclear. Chapter 4 of this dissertation describes the identification and characterization of a previously unknown BvgAS regulated virulence factor, the immunoglobulin binding autotransporter, BatB. Only B. bronchiseptica produces a functional BatB protein, suggesting the presence of BatB may be detrimental to human infection and therefore involved in determining host specificity.