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ABSTRACT Plants have coevolved with herbivorous insects for millions of years, resulting in variation in resistance both within and between species. Using a manipulative experiment combined with untargeted metabolomics, microbiome sequencing and transcriptomics approaches, we investigated the roles of plant metabolites and the microbiome in defence mechanisms in native resistant Manchurian ash (Fraxinus mandshurica) trees and non‐native susceptible velvet ash (Fraxinus velutina) trees against the highly invasive emerald ash borer (EAB,Agrilus planipennis). Comparative transcriptomics and metabolomics analyses show that the phenylpropanoid pathway, which is enriched in differentially expressed genes and differentially abundant metabolites, may serve as a potential regulator of resistance. Additionally, the microbiome is distinctly shifted in two ash species. Indicator taxa analysis reveals that the distinct genera are dominant in the galleries of two ash species, for example,Pseudomonasin velvet, andHafnia‐Obesumbacteriumin Manchurian. The strong correlation between indicator taxa and metabolites suggests that the chemical compounds might impact the microbial community in phloem directly or indirectly, or vice versa. This study significantly enhances our understanding of the variation in resistance between ash species and its contribution to the invasion success of EAB, providing valuable insights for the development of pest management strategies.