Plant-associated bacteria encounter a range of stressful environmental conditions when colonizing leaf surfaces. To adapt to these harsh conditions bacteria sense and respond to environmental signals. Within the last two decades, photoreceptors that respond to specific wavelengths of light through associated chromophores have been discovered with increasing frequency in non-photosynthetic bacteria, including those associated with plants. Their presence suggests that fluctuations in light may serve as a cue to regulate bacterial adaptations. The foliar plant pathogen Pseudomonas syringae is unusual among heterotrophic bacteria because it encodes three photoreceptors, two red- and/or far-red light-sensing bacteriophytochromes and a blue light-sensing LOV protein. Here we evaluated the physiological roles of these photoreceptors, their mechanisms of regulation, and their impacts on plant colonization. This work provides the first evidence in bacteria for an integrated signaling network composed of both a LOV protein and a phytochrome, and shows that the bacteriophytochrome, BphP1, and LOV control swarming motility. BphP1 represses swarming motility in response to red and far-red light, whereas LOV attenuates BphP1-mediated repression. Moreover, this is the first bacteriophytochrome shown to have blue-light sensing capabilities, and these occur independently of red-light sensing. Furthermore, this work identifies a role for a bacteriophytochrome in plant colonization for the first time and demonstrates that this bacteriophytochrome, BphP1, promotes survival during the initial stages of leaf colonization and negatively regulates colonization later on. BphP1-mediated regulation of swarming motility is associated with the ability of P. syringae to move from soil to seeds and contributes to lesion development. This work further elucidates the mechanism of BphP1-mediated regulation and demonstrates that BphP1 and a regulator we designate Lsr repress swarming motility in response to red light by controlling the transition from a sessile to motile lifestyle. Additionally, an acyl-homoserine lactone molecule functions as a downstream component in this signal transduction pathway. This work also provides evidence for light-mediated regulation of the type IV pilus and demonstrates for the first time a role for type IV pili in the swarming motility of P. syringae pv. syringae. Furthermore, the global regulator AlgU is shown to negatively regulate swarming independent of alginate production, which itself enhances swarming motility. Finally, the work documents an unusual interaction between P. syringae colonies that manifests as induced movement away from colonies producing the repellent 3-(3-hydroxyalkanoyloxy) alkanoic acid by strain derivatives that otherwise appear non-motile.