The coevolution between insect vectors and pathogens has long been of interest in molecular ecology and evolutionary biology, and Diaphorina citri is the main insect vector of the bacterium, ‘Candidatus Liberibacter asiaticus’ (CLas), the putative cause of the severe Asian form of huanglongbing. CLas-positive D. citri are more fecund than their CLas-negative counterparts; however, the molecular mechanism underlying of increased fecundity remains unclear. Here, we found that CLas promoted ovarian development and increased the expression of the vitellogenin receptor (DcVgR) in ovaries. DcVgR RNAi significantly decreased fecundity and CLas titer in ovaries, extended the preoviposition period, shortened the oviposition period, and blocked ovarian development. Combined in vivo and in vitro experiments showed that miR-275 suppressed DcVgR expression by binding to its 3’ untranslated region. Overexpression of miR-275 resulted in a decline of DcVgR expression and CLas titer in ovaries and caused reproductive defects that mimicked DcVgR knockdown phenotypes. After infection with CLas, the juvenile hormone (JH) signaling pathway was upregulated thereby increasing DcVgR expression via the JH receptor, methoprene-tolerant (Met), and downstream key transcription factor Krüppel homolog 1. As a result, CLas hijacks the JH signaling pathway and host miR-275 that targets DcVgR to improve D. citri fecundity, while simultaneously increasing the replication of CLas itself, suggesting a mutualistic interaction in D. citri ovaries with CLas.