Dog-infecting haemotropic mycoplasmas (haemoplasmas), such asMycoplasmahaemocanisandCandidatusMycoplasma haematoparvum are common blood-borne pathogens of canines that can potentially inflict a substantial burden of disease, particularly in immunosuppressed individuals. Nonetheless, the transmission of these pathogens remains debated as more evidence emerges that they may not be transmitted by vectors, but instead use alternative methods such as aggressive interactions and vertical transmission. Here, we treated forty dogs with two different topically-acting ectoparasiticide products able to prevent vector-borne pathogen infections during an 8-month community trial in Cambodia. A total absence of ectoparasites were observed at all time points, and no new infections caused by pathogens confirmed as being vectorially-transmitted were detected, i.e.,Babesiavogeli,Ehrlichiacanis,Anaplasmaplatys, andHepatozooncanis. Conversely, the number of haemoplasma infections in dogs on both ectoparasiticides rose significantly, with an incidence of 26 infections per 100 dogs at risk per year, providing strong evidence of non-vectorial transmission. Over the study period, dog aggression and fighting were frequently observed, highlighting a different potential mode of transmission. This study presents the first robust evidence that canine haemoplasmas may be transmitted without arthropod vectors drawing attention to the need for new methods to prevent their transmission.