The molecular interactions between the Asian citrus psyllid and ‘Candidatus Liberibacter asiaticus’ (CLas) is a critical area of citrus greening research. In this work, we used high resolution mass spectrometry to measure the collection of small, native proteins found in the psyllid (the peptidome), and discovered evidence for multiple classes of bioactive peptides that are up- or down-regulated in CLas-infected psyllids as compared to non-infected psyllids. Psyllid peptides with strong sequence and structural homology to insect neuropeptides were identified, and remarkably, 10 of the 13 neuropeptide precursors identified were down-regulated in CLas-infected insects. Oral delivery of two neuropeptide analogs to the psyllid from artificial diets induced wing deformities and high levels of mortality in adult psyllids. In addition, a series of candidate peptide biomarkers that predict the CLas-infection state of psyllids were identified. A total of 15 candidate biomarkers, which were found consistently up-regulated in or unique to CLas-infected insects, resemble known antimicrobial peptides (AMPs). These candidate AMPs have been synthesized and will be tested for activity against a panel of bacteria, including the only culturable species of Liberibacter, L. crescens. Taken together, the information obtained in this work not only yields new insights into psyllid physiology and multitrophic interactions, but may also lead to the development of novel diagnostic and management tools for citrus greening disease.