Background <p>Sri Lanka is experiencing a re-emergence of brugian filariasis 4 decades after its elimination in 1969. A comprehensive understanding of the mosquito species that can facilitate the development of the brugian parasite is essential for implementing targeted surveillance and control measures. This study evaluated the vector potentiality of field-caught mosquitoes for brugian parasites across endemic districts within the filarial transmission belt in Sri Lanka.</p> Methods <p>Mosquito surveillance was conducted at six sites across five districts with the highest reported brugian cases during 2021–2022. Mosquitoes were collected at the site of the most recently reported human brugian case in each district using dog-baited, window and gravid traps to maximize species diversity and abundance in the sample. Mosquitoes were identified morphologically, and randomly selected mosquitoes were molecularly confirmed via a PCR targeting the <i>COΙ</i> region. Vector potentiality was evaluated by observing nematode parasites upon dissection, molecular confirmation via PCR and sequencing the <i>Brugia sp.</i>-specific <i>HhaΙ</i> region. Mosquitoes harboring the infective L3 stage brugian parasites were tested for the presence of human DNA to investigate their involvement in human brugian filariasis transmission. Statistical analyses were performed using generalized linear mixed models.</p> Results <p>A total of 766 mosquitoes of 15 species were dissected to obtain L3 larvae of the brugian parasite. Of these, 10.05% (<i>n</i> = 77) from nine species across four genera were identified to support the development of <i>Brugia</i> spp. to the infective L3 larval stage within the head and thoraces of field-caught mosquitoes: <i>Mansonia annulifera, Ma. indiana, Ma. uniformis</i>, <i>Culex lophoceraomyia, Cx. tritaeniorhynchus</i>, <i>Cx. quinquefasciatus</i>, <i>Cx. vishnui</i>, <i>Armigeres subalbatus</i> and <i>Coquillettidia crassipes.</i> Notably, <i>Ma. indiana</i>, which has not previously been identified as a potential vector for brugian filariasis in Sri Lanka, showed the highest weighted infectivity at the S₁ site. Site-based risk assessment identified the S₁ site as having the highest risk of brugian filariasis followed by S₆.</p> Conclusions <p>Many mosquito genera supporting the development of <i>Brugia</i> spp. to the infective L3 larval stage in field-caught mosquitoes were identified expanding beyond the previously known <i>Mansonia</i> vectors. The diversity of potentially infective species indicates complex transmission dynamics requiring integrated surveillance approaches.</p>