The diversity and prevalence of canine vector-borne pathogens (VBPs) in Bhutan have to date remained unexplored, whilst recent epidemiological surveys in other South Asian nations have found diseases caused by VBPs to be rife in local dog populations. Importantly, many of such VBPs can infect people as well, with a building body of evidence identifying potentially zoonotic rickettsial organisms infecting humans in Bhutan. Given the lack of data on canine pathogens in Bhutan we employed a suite of deep-sequencing metabarcoding methods using Oxford Nanopore Technologies' MinION™ device to holistically characterise the bacterial, apicomplexan and filarial worm blood-borne pathogens of dogs in the country's south. Of the 95 stray, owned and community dogs sampled 78% (95% CI = 69%-85%) were infected with at least one VBP. Pathogen species detected were highly diverse including the bacteria in 16% (95% CI: 10-24%), in 4% (95% CI: 2-10%), in 2% (95% CI: 0.5-7%) of dogs as well as the zoonotic species in 1% (95% CI: 0.1-6%), a potentially novel spp. and an -like bacterium, both in 1% (95% CI: 0.1-6%) of dogs. The apicomplexan haemoparasites in 62% (95% CI: 52-71%), in 45% (95% CI: 36-55%) and in 3% (95% CI: 1-9%) of dogs were also detected. Finally, 5% (95% CI: 2-12%) of dogs were found to be infected with the filarioid and 1% (95% CI: 0.1-6%) with zoonotic sp. hongkongensis. One canine was found positive to the filarioid , a species normally found infecting cervids. The elucidated diversity of VBP communities highlights the strength of assumption-free diagnostics, such as metabarcoding, in detecting rare, novel, and unexpected pathogens. This approach to identifying pathogen diversity is of critical importance when investigating regions and populations that have thus far been neglected, with the findings aiding the development of future One Health informed strategies for disease control.