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Flavone is widely found in plants and plays an important role in plant defense against pests. Many pests, such as <i>Helicoverpa armigera</i>, use flavone as a cue to upregulate counter-defense genes for detoxification of flavone. Yet the spectrum of the flavone-inducible genes and their linked <i>cis</i>-regulatory elements remains unclear. In this study, 48 differentially expressed genes (DEGs) were found by RNA-seq. These DEGs were mainly concentrated in the retinol metabolism and drug metabolism-cytochrome P450 pathways. Further in silico analysis of the promoter regions of 24 upregulated genes predicted two motifs through MEME and five previously characterized <i>cis</i>-elements including CRE, TRE, EcRE, XRE-AhR and ARE. Functional analysis of the two predicted motifs and two different versions of ARE (named ARE1 and ARE2) in the promoter region of the flavone-inducible carboxylesterase gene <i>CCE001j</i> verified that the two motifs and ARE2 are not responsible for flavone induction of <i>H. armigera</i> counter-defense genes, whereas ARE1 is a new xenobiotic response element to flavone (XRE-Fla) and plays a decisive role in flavone induction of <i>CCE001j</i>. This study is of great significance for further understanding the antagonistic interaction between plants and herbivorous insects.