We investigated the ability of Hymenoscyphus fraxineus mitovirus 1 (HfMV1) to spread in nature through the airborne inoculum of its fungal host, the devastating Hymenoscyphus fraxineus. Eight rotating-arm spore traps were installed to collect the airborne spores (presumably ascospores) of H. fraxineus in four ecologically different ash forests in the Czech Republic. Spore trap samples were subjected to direct DNA and RNA extractions and subsequent qPCR and mitovirus-specific reverse transcription (RT) qPCR for detection and quantification of H. fraxineus and HfMV1, respectively. The prevalence of HfMV1 was confirmed in 57% of H. fraxineus sampled inocula, showing that its occurrence is significantly correlated with its fungal host H. fraxineus. Furthermore, the ratio of mitovirus carrying spores was shown to be constant at any level of H. fraxineus infection pressure independently of the studied locality. Temperatures of 19–21°C at the time of spore trapping correlated with the highest levels of both HfMV1 and H. fraxineus. Our data confirm H. fraxineus airborne inoculum as an efficient transport means for HfMV1 in nature. Moreover, this research uses a new technology to directly study a mycovirus through its host aerospora.