Pathogens face numerous challenges to persist in hosts with low or unpredictable population densities. Strategies include horizontal transmission, such as by the production of propagules that persist in the environment, and vertical transmission from adults to offspring. While many pathogens are capable of horizontal and vertical transmission little is known of their relative roles under realistic conditions of changing population densities. Insect baculoviruses can be transmitted both horizontally and vertically, although much of the work on baculovirus transmission has focussed on horizontal transmission that can be effective at high host densities. Here, we examine the prevalence of a vertically-transmitted, covert infection of nucleopolyhedrovirus (NPV) in field populations of the African armyworm, Spodoptera exempta, in Tanzania. African armyworm is a major pest of graminaceous crops in Africa and despite its migratory nature and boom and bust dynamics, NPV epizootics are common and can be intense at the end of the multi-generation armyworm season. We found that virtually all the insects collected in the field were positive for S. exempta NPV (SpexNPV) DNA and 60% of these insects had transcriptionally active virus. This suggests that SpexNPV is transmitted vertically at extremely high levels in field populations of S. exempta and can maintain a persistent infection without obvious symptoms. Similarly high levels of virus DNA and RNA were detected in a S. exempta colony that had been maintained in continuous culture for 5 years. This study provides an insight into mechanisms of pathogen persistence in migratory populations where hosts are unpredictable and indicates that covert infection may be more common and more relevant in disease dynamics of insects than had previously been thought.