Parasite infrapopulation size – the population of parasites affecting a single host – is a central metric in parasitology. However, parasites are small and elusive such that imperfect detection is expected. Repeated sampling of parasites during primary sampling occasions (e.g., each host capture) informs the detection process. Here, we estimate flea (Siphonaptera) infrapopulation size on black-tailed prairie dogs (Cynomys ludovicianus, BTPDs) as a proof-of-concept for estimating parasite infrapopulations given imperfect detection. From Jun-Aug 2011, we live-trapped 299 BTPDs for a total of 573 captures on 20 plots distributed among 13 colonies at the Vermejo Park Ranch, New Mexico, USA. During each capture, an anesthetized BTPD was combed 3 times consecutively, 15 s each, to remove and count fleas. Each flea (n = 4846) was linked to the BTPD from which it was collected and assigned an encounter history (‘100’, ‘010’, ‘001’). We analyzed the encounter histories using Huggins closed captures models, setting recapture probabilities to 0, thereby accounting for flea removal from hosts. The probability of detecting an individual flea (p) increased with Julian date; field personnel may have become more efficient at combing fleas as the field season progressed. Combined p across 3 combings equaled 0.99. Estimates of flea infrapopulation size were reasonable and followed the negative binomial distribution. Our general approach may be broadly applicable to estimating infrapopulation sizes for parasites. The utility of this approach increases as p declines but, if p is very low, inference is likely limited.