Bacteria use diffusible chemical signals to communicate within and between species and to coordinate certain group behaviors, including expression of host colonization factors. For Vibrio fischeri, a bioluminescent bacterium that colonizes the Hawaiian bobtail squid Euprymna scolopes, bioluminescence is required to colonize the host fully, and it is controlled in part by the pheromone-dependent LuxR-LuxI regulatory system. While pheromone-dependent luminescence induction is influenced by cell density, V. fischeri cells in culture are ~1000 times less luminescent and produce less pheromone than symbiotic cells, despite being at similar high cell densities. These observations and others suggest that density-independent factors also govern LuxR-LuxI mediated pheromone signaling. In this dissertation I describe how certain environmental cues regulate the LuxR-LuxI regulatory system to control both pheromone production and bioluminescence in V. fischeri. I show evidence that the squid light organ is a low iron environment and that low iron stimulates early induction and overall brighter luminescence in V. fischeri ES114 in culture. Moreover I demonstrate that inactivation of the redox-responsive ArcA/ArcB two-component regulatory system derepresses pheromone production, initiating a positive feedback loop wherein pheromone can diffuse into surrounding cells to stimulate more pheromone synthesis and induce bright luminescence. I also describe how oxygen levels influence luminescence through the oxygen-sensitive transcriptional regulator FNR, which regulates anaerobic respiration in V. fischeri in addition to bioluminescence. Finally, I show that citrate, a primary metabolite, regulates luminescence and this pathway requires the Gac/Csr regulatory cascade, which is conserved throughout proteobacteria and is a known regulator of both central carbon metabolism and host colonization factors. These findings show in greater detail how pheromone-mediated regulation in V. fischeri is governed by more than cell density alone, and they suggest that pheromones can convey information about specific conditions, such as changes in redox or carbon flow, in addition to population size. This dissertation broadens our perspective of bacterial pheromone-mediated communication and bacterial gene regulation in natural infections.