Abstract Granuloviruses are insect viruses commonly used as biological insecticides for pest control in agriculture. Most pest control programs rely on the most virulent strains and doses to cause acute mortality events. However, we hypothesize that sublethal infections are key to maintaining persistent epidemics that regulate pest populations in the long‐term. The tomato leafminer (TLM), Tuta absoluta (Meyrick) (= Phthorimaea absoluta Meyrick) (Lepidoptera: Gelechiidae), is one of the most limiting pests of greenhouse and field tomatoes. Previous efforts have identified a strain of Phthorimaea operculella granulovirus (PhopGV), coded VG013, associated with field populations of the TLM, which causes significant acute mortalities and is being used as active ingredient of a biological insecticide. The aim of this study was to determine the effect of sublethal infections and transmission mechanisms of PhopGV‐VG013 on TLM populations. Six viral doses were tested for their virulence and effects on TLM development rate, and intrinsic population growth rate. A sublethal dose was selected to compare the density‐dependent mortality of TLM populations and vertical transmission was examined by testing for PhopGV in the offspring of surviving infected individuals. Horizontal transmission was assessed by testing for PhopGV in frass of infected larvae, and the infection of virus‐free larvae confined with infected larvae in the same leaf. We found that sublethal doses of PhopGV have slight effects on TLM population growth rates, and none on the strength of density‐dependent mortality. Although we found for the first time that PhopGV‐VG013 is transmitted to approximately 7.5% of the offspring of individuals that survive the virus challenge, we found no evidence suggesting horizontal transmission from sublethal infections. Our results show that sublethal infections of highly virulent ganulovirus strains may favor long‐term pathogen persistence but have a limited role in host population regulation.