Peptidoglycan recognition proteins (PGRPs) are evolutionarily conserved molecules. Their role in the immune response to invading pathogens makes them a natural target for viral defence study in a wide range of organisms. Silverleaf whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) is one of the invasive insect pests and transmits begomoviruses in a circulative and persistent manner to vegetables, legumes, fibres and ornamentals. The virus entry, retention, circulation, and release process involve interactions with several proteins in B. tabaci and evade innate immunity to avoid the antiviral mechanisms. The present study investigated the role of BtPGRP in chilli leaf curl virus (ChiLCV, Begomovirus capsica) transmission by B. tabaci. Silencing of BtPGRP using double-stranded (ds) RNA led to the loss of innate immunity to ChiLCV resulting in increased virus titre in B. tabaci. dsBtPGRP was orally administered to adults of B. tabaci at a concentration of 1, 3, and 5 ug/mL. The expression of BtPGRP was downregulated up to 4.67-fold. The virus titre in B. tabaci increased 90.05 times post-exposure to dsBtPGRP at 5 μg/mL. The test plants inoculated with ChiLCV by dsBtPGRP-exposed B. tabaci expressed severe curling symptoms with a higher virus load and transmission ratio than the control. Besides, the silencing of BtPGRP also induced up to 56.67% mortality in treated B. tabaci. The active site pocket of BtPGRP was found to interact directly with the ChiLCV-CP in computational analyses. Key residues of BtPGRP, including Tyr45, Asp84, His86, Trp87, and Asn119 exhibited critical interaction with the ChiLCV-CP. To our knowledge, this is the first report on the effect of PGRP silencing on ChiLCV acquisition and transmission by B. tabaci Asia II I and its fitness.