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Nicotine is one of the most toxic secondary plant metabolites in nature and it is highly toxic to herbivorous insects. The overexpression of <i>CYP6CY3</i> and its homologous isozyme <i>CYP6CY4</i> in <i>Myzus persicae nicotianae</i> is correlated with nicotine tolerance. The expanded (AC)_n repeat in promoter is the <i>cis</i> element for <i>CYP6CY3</i> transcription. These repeat sequences are conserved in the <i>CYP6CY3</i> gene from <i>Aphis gossypii</i> and the homologous P450 genes in <i>Acyrthosiphon pisum</i>. The potential transcriptional factors that may regulate <i>CYP6CY3</i> were isolated by DNA pulldown and sequenced in order to investigate the underlying transcriptional regulation mechanism of <i>CYP6CY3</i>. These identified transcriptional factors, <i>AhR</i> and <i>ARNT</i>, whose abundance was highly correlated with an abundance of the <i>CYP6CY3</i> gene, were validated. RNAi and co-transfection results further confirm that <i>AhR</i> and <i>ARNT</i> play a major role in the transcriptional regulation of the <i>CYP6CY3</i> gene. When the <i>CYP6CY3</i> transcript is destabilized by <i>AhR/ARNT</i> RNAi, the transcription of the <i>CYP6CY4</i> is dramatically up-regulated, indicating a compensatory mechanism between the <i>CYP6CY3</i> and <i>CYP6CY4</i> genes. Our present study sheds light on the <i>CYP6CY3</i> and <i>CYP6CY4</i> mediated nicotine adaption of <i>M. persicae nicotianae</i> to tobacco. The current studies shed light on the molecular mechanisms that underlie the genotypic and phenotypic changes that are involved in insect host shifts and we conclude that AhR/ARNT regulate the expression of <i>CYP6CY3</i> and <i>CYP6CY4</i> cooperatively, conferring the nicotine adaption of <i>M. persicae nicotianae</i> to tobacco