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<i>Camptotheca acuminata</i> Witches’-broom disease (CaWB) is the most destructive disease affecting <i>C. acuminata</i> in China. Previous studies on CaWB have failed to clarify the incidence pattern in <i>C. acuminata</i> after infection with phytoplasma. The time interval between phytoplasma infection of <i>C. acuminata</i> and the onset of Witches’-broom symptoms in <i>C. acuminata</i> was very long. <i>C. acuminata</i> inoculated with CaWB showed leaf margin scorching symptoms at 4 weeks in inoculated leaves. At 16 weeks after infection (WAI), old leaves were shed, while new leaves showed a mild leaf margin scorch; at 28 WAI, typical symptoms appeared. Transcriptomic and metabolomic analyses of the three sampling periods revealed 194 differentially expressed genes, mainly enriched in MAPK signaling, plant–pathogen interaction, phenylpropanoid biosynthesis, starch and phenylpropanoid biosynthesis, and phenylpropanoid biosynthesis pathways. The expression of calcium-dependent protein kinase (CDPK), β Ketoacyl-CoA Synthase1/10 (KCS1/10), and WRKY22/29 genes in the plant–pathogen interaction pathway significantly increased, indicating that they may be key genes in the CaWB phytoplasma-mediated maintenance of ROS homeostasis. Moreover, isochlorogenic acid B, atractylenolide II, and 3-methoxybenzoic acid were found, which might serve as signaling or functional substances in the defense response. Our results provide novel insights into the pathogenesis of CaWB and the defense response of <i>C. acuminata</i> under the influence of phytoplasma. Additionally, we identified potential candidate genes related to the defense response of <i>C. acuminata</i>, laying the foundation for further research.