Many pathogenic bacteria with different lifestyles can proliferate and colonize the phyllosphere. To ensure successful colonization, these bacterial pathogens employ several virulence strategies to evade plant tissues, suppress plant immunity, and obtain essential nutrients to promote their population growth. Various small molecules secreted by pathogens are key success factors contributing to their survival in the phyllosphere. However, the molecular mechanisms underlying several of these molecules are not well understood. Thus, the goal of this dissertation was to decipher the mechanistic connections of bacterial small molecules during plant colonization. In Chapter I, I review the distinct lifestyles of foliar pathogens as they adapt to plant hosts and emphasize the significance of small molecule signaling in bacterial pathogenesis success. The scope of this review provided the framework for Chapters 2 and 3, in which I investigated the impact of small molecule signaling on bacterial virulence during plant colonization. In Chapter 2, I functionally characterized a set of genes responsible for the quorum sensing (QS) molecule N-acyl homoserine lactone (AHL) in a plant pathogen model, Pseudomonas syringae pv. tomato (Pst) DC3000. These findings revealed the requirement of AHL for the full virulence and fitness of Pst DC3000. Finally, in Chapter 3, I employed a metabolomic-based method to identify metabolites that have a significant impact during plant-pathogen interactions on the leaf surface environment. Moreover, these data indicate clear differences in metabolic dynamics between a plant pathogen and a human pathogen. Altogether, my work has significantly contributed to the growing research field of small molecule signaling in bacteria, which interconnects with other regulatory networks to control bacterial physiology and pathogenicity.