‘
Candidatus
Liberibacter asiaticus’ (
C
Las), the causal agent of citrus huanglongbing, is transmitted by the Asian citrus psyllid
Diaphorina citri
. While
C
Las-positive (
C
Las+) females exhibit increased fecundity and metabolic demands, their neuroendocrine regulation mechanisms remain unclear. We propose
C
Las manipulates dopamine (DA) signaling to enhance psyllid fecundity and
C
Las proliferation. Metabolomics revealed elevated DA in
C
Las+ females. Silencing DA synthesis genes and receptor
DcDop2
via RNAi reduced lipid reserves, fecundity, and ovarian
C
Las titers. Through combined
in vivo
and
in vitro
experiments, we demonstrated that the microRNA miR-31a suppresses
DcDop2
expression by binding to its 3’ untranslated region. Overexpression of miR-31a resulted in decreased
DcDop2
expression and
C
Las titers in the ovaries, eliciting phenotypic defects akin to
DcDop2
knockdown. Furthermore,
DcDop2
knockdown and miR-31a overexpression reduced juvenile hormone (JH) levels and adipokinetic hormone (AKH) signaling in fat bodies and ovaries. Consequently,
C
Las regulates the DA-
DcDop2
signaling axis to improve
D. citri
lipid metabolism and fecundity, while simultaneously promoting its replication. These findings reveal a coevolution between
C
Las proliferation and ovarian development in the insect host. This discovery enhances our understanding of the molecular interplay between plant pathogens and vector insects and offers novel targets and strategies for HLB field management.