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Abstract As populations differentiate across geographic or host‐association barriers, interpopulation fertility is often a measure of the extent of incipient speciation. The bed bug,Cimex lectulariusL., was recently found to form two host‐associated lineages within Europe: one found with humans (human‐associated, HA) and the other found with bats (bat‐associated, BA). No unequivocal evidence of contemporary gene flow between these lineages has been found; however, it is unclear whether this is due to an inability to produce viable “hybrid” offspring. To address this question and determine the extent of compatibility between host‐associated lineages, we set up mating crosses among populations of bed bugs based on both their host association (human—HA vs. bat—BA) and geographic origin (North America vs. Europe). Within‐population fecundity was significantly higher for all HA populations (>1.7 eggs/day) than for BA populations (<1 egg/day). However, all within‐population crosses, regardless of host association, had >92% egg hatch rates. Contrary to previous reports, in all interlineage crosses, successful matings occurred, fertile eggs were oviposited, and the F₁“hybrid” generation was found to be reproductively viable. In addition, we evaluated interpopulation genetic variation inWolbachiaamong host‐associated lineages. We did not find any clear patterns related to host association, nor did we observe a homogenization ofWolbachialineages across populations that might explain a breakdown of reproductive incompatibility. These results indicate that while the HA and BA populations ofC. lectulariusrepresent genetically differentiated host‐associated lineages, possibly undergoing sympatric speciation, this is in its incipient stage as they remain reproductively compatible. Other behavioral, physiological, and/or ecological factors likely maintain host‐associated differentiation.