BACKGROUND The northern fowl mite (NFM; Ornithonyssus sylviarum) is a blood-feeding ectoparasite of birds and a major pest of poultry in the United States. Mite populations spread rapidly in commercial flocks, reach peak burdens of >70,000 mites per bird and have developed resistance to many pesticides. Despite decades as a pest in the United States, the reproductive biology of NFM remains unclear. Based on karyotypes, the NFM has haplodiploid sex determination, which suggests unmated females could produce male offspring (arrhenotoky). Thus, unmated females could disseminate to a new host and initiate an infestation by producing and mating with sons (oedipal mating). METHODS We used small capsules to isolate and recover NFM on host chickens. Mites in capsules could blood feed, develop and reproduce, but could not contact other mites. Individual larvae were matured in isolation to produce known, unmated females. We evaluated reproduction of (I) previously mated females (i) in isolation, or (ii) paired with a male, and (II) unmated (virgin) females in isolation. In each treatment we recorded the number and sexes of offspring produced over time. RESULTS Mated NFM produced female and male offspring in isolation, or when paired with a male. When paired with a male, females produced a female-biased sex ratio of the offspring (F:M ratio ~5:1). Unmated, female NFM produced exclusively male offspring when in isolation. When paired with their sons that had developed to maturity, the "virgin" females were able to mate and subsequently produce female offspring. CONCLUSIONS This study found that females with immediate access to sperm produced mostly female offspring. Virgin female NFM initially produced only male offspring and subsequently used oedipal mating to produce female offspring. Using this reproductive system NFM could successfully colonize new hosts as immature, or unmated females. The strong female-biased sex ratio of NFM populations suggests a large proportion of the parasite population is capable of disseminating to new hosts, which is essential for an obligate parasite to persist.