Climate change is predicted to increase the prevalence of vector-borne disease due to expansion of insect populations. ‘ Candidatus Liberibacter solanacearum’ is a phloem-limited pathogen associated with multiple economically important diseases in solanaceous crops. Little is known about the strategies and pathogenicity factors ‘ Ca. L. solanacearum’ uses to colonize its vector and host. We determined the ‘ Ca. L. solanacearum’ effector repertoire by predicting proteins secreted by the general secretory pathway across four different ‘ Ca. L. solanacearum’ haplotypes, investigated effector localization in planta, and profiled effector expression in the vector and host. The localization of ‘ Ca. L. solanacearum’ effectors in Nicotiana spp. revealed diverse eukaryotic subcellular targets. The majority of tested effectors were unable to suppress plant immune responses, indicating they possess unique activities. Expression profiling in tomato and the psyllid Bactericera cockerelli indicated ‘ Ca. L. solanacearum’ differentially interacts with its host and vector and can switch effector expression in response to these environments. This study reveals ‘ Ca. L. solanacearum’ effectors possess complex expression patterns, target diverse host organelles and the majority are unable to suppress host immune responses. A mechanistic understanding of ‘ Ca. L. solanacearum’ effector function will reveal novel targets and provide insight into phloem biology. [Formula: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license .