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Strongyloidiasis is a much-neglected soil born helminthiasis caused by the nematode Strongyloides stercoralis. Human derived S. stercoralis can be maintained in dogs in the laboratory and this parasite has been reported to also occur in dogs in the wild. Some authors have considered strongyloidiasis a zoonotic disease while others have argued that the two hosts carry host specialized populations of S. stercoralis and that dogs play a minor role, if any, as a reservoir for zoonotic S. stercoralis infections of humans. We isolated S. stercoralis from humans and their dogs in rural villages in northern Cambodia, a region with a high incidence of strongyloidiasis, and compared the worms derived from these two host species using nuclear and mitochondrial DNA sequence polymorphisms. We found that in dogs there exist two populations of S. stercoralis, which are clearly separated from each other genetically based on the nuclear 18S rDNA, the mitochondrial cox1 locus and whole genome sequence. One population, to which the majority of the worms belong, appears to be restricted to dogs. The other population is indistinguishable from the population of S. stercoralis isolated from humans. Consistent with earlier studies, we found multiple sequence variants of the hypervariable region I of the 18 S rDNA in S. stercoralis from humans. However, comparison of mitochondrial sequences and whole genome analysis suggest that these different 18S variants do not represent multiple genetically isolated subpopulations among the worms isolated from humans. We also investigated the mode of reproduction of the free-living generations of laboratory and wild isolates of S. stercoralis. Contrary to earlier literature on S. stercoralis but similar to other species of Strongyloides, we found clear evidence of sexual reproduction. Overall, our results show that dogs carry two populations, possibly different species of Strongyloides. One population appears to be dog specific but the other one is shared with humans. This argues for the strong potential of dogs as reservoirs for zoonotic transmission of S. stercoralis to humans and suggests that in order to reduce the exposure of humans to infective S. stercoralis larvae, dogs should be treated for the infection along with their owners., Author summary Infections of humans with the nematode Strongyloides stercoralis can persist for a very long time, due to the capacity of this pathogen to undergo an autoinfective life cycle and re-infect the same host over and over again. Clinical manifestation, known as human stongyloidiasis, may be fatal and can arise many years and generations of worms after the initial infection occurred. Although Strongyloides stercoralis has been known as the causative agent of strongyloidiasis for a very long time, some key questions about its biology and epidemiology remain open. Here we address two of them. Firstly, it has long been known that dogs can serve as experimental hosts for S. stercoralis but it is a matter of debate whether Strongyloides spp. found in dogs in the wild are human pathogenic S. stercoralis, and whether dogs therefore are a source of zoonotic transmission of this parasite. Here we show that dogs carry two genetically different populations of Strongyloides spp. one of which is shared with humans. This demonstrates that dogs represent a possible reservoir for zoonotic strongyloidiasis. Secondly, the all female, parthenogenetic parasitic generations may alternate with single facultative free-living generations, which consist of both females and males. In spite of the presence of both sexes, it had been postulated that males do not contribute genetic material to the progeny and that sperm are merely required to trigger parthenogenetic embryonic development. Here we show that the free-living adults of S. stercoralis reproduce sexually.