The viruses that cause dengue fever, Zika and chikungunya are transmitted by the mosquito, Aedes aegypti and threaten global public health. Current vaccines and treatments against these viruses along with methods of mosquito control are of limited efficacy and novel interventions are needed. Wolbachia are bacteria that inhabit insect cells and have been found to reduce viral infection, a phenotype that is referred to as viral ‘blocking’. Although not naturally found in A. aegypti, Wolbachia were stably introduced into this mosquito in 20115 and have been shown to reduce the transmission potential of dengue, Zika and chikungunya. Trials in the tropics show that Wolbachia can spread through A. aegypti populations and reduce the local incidence of dengue fever. Despite this, the stability of viral blocking over time is unknown. Here, we reveal genes in A. aegypti that appear to affect the strength of Wolbachia-mediated dengue blocking in response to selection. We find that mosquito genotypes associated with weaker dengue blocking have reduced fitness, suggesting that there is potential for blocking to be maintained by selection. These results will inform the use of Wolbachia as biocontrol agents against mosquito-borne viruses and direct further research into measuring and improving their efficacy.