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The internal microbiome of common cat and dog fleas was studied for DNA evidence of pathogenic bacteria. Fleas were grouped in pools by parasitized animal. DNA was extracted and investigated with 16S metagenomics for medically relevant (MR) bacteria, based on the definitions of the International Statistical Classification of Diseases and Related Health Problems (WHO). The MR bacterial species totaled 40, were found in 60% of flea-pools (N = 100), and included <i>Acinetobacter</i><i>baumannii</i>, <i>Bacteroides</i><i>fragilis</i>, <i>Clostridium</i><i>perfringens</i>, <i>Enterococcus</i><i>faecalis</i>, <i>E</i>. <i>mundtii</i>, <i>Fusobacterium</i><i>nucleatum</i>, <i>Haemophilus</i><i>aegyptius</i>, <i>Kingella</i><i>kingae</i>, <i>Klebsiella</i><i>pneumoniae</i>, <i>Leptotrichia</i><i>buccalis</i>, <i>L</i>. <i>hofstadii</i>, <i>Moraxella</i><i>lacunata</i>, <i>Pasteurella</i><i>multocida</i>, <i>Propionibacterium</i><i>acnes</i>, <i>P</i>. <i>propionicum</i>, <i>Proteus</i><i>mirabilis</i>, <i>Pseudomonas</i><i>aeruginosa</i>, <i>Rickettsia</i><i>australis</i>, <i>R</i>. <i>hoogstraalii</i>, <i>Salmonella</i><i>enterica</i>, and various <i>Bartonella</i>, <i>Staphylococcus</i>, and <i>Streptococcus</i> species. <i>B</i>. <i>henselae</i> (<i>p</i> = 0.004) and <i>B</i>. <i>clarridgeiae</i> (<i>p</i> = 0.006) occurred more frequently in fleas from cats, whereas <i>Rickettsia</i><i>hoogstraalii</i> (<i>p</i> = 0.031) and <i>Propionibacterium</i><i>acnes</i> (<i>p</i> = 0.029) had a preference in fleas from stray animals. Most of the discovered MR species can form biofilm, and human exposure may theoretically occur through the flea-host interface. The fitness of these pathogenic bacteria to cause infection and the potential role of fleas in the transmission of a broad range of diseases should be further investigated.