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For the development of sustainable control of tick-borne diseases, insight is needed in biological factors that affect tick populations. Here, the ecological interactions among <i>Ixodiphagus hookeri</i>, <i>Ixodes ricinus</i>, and two vertebrate species groups were investigated in relation to their effects on tick-borne disease risk. In 1129 questing ticks, <i>I. hookeri</i> DNA was detected more often in <i>I. ricinus</i> nymphs (4.4%) than in larvae (0.5%) and not in adults. Therefore, we determined the infestation rate of <i>I. hookeri</i> in nymphs from 19 forest sites, where vertebrate, tick, and tick-borne pathogen communities had been previously quantified. We found higher than expected co-occurrence rates of <i>I. hookeri</i> with deer-associated <i>Anaplasma phagocytophilum</i>, and lower than expected rates with rodent-associated <i>Borrelia afzelii</i> and <i>Neoehrlichia mikurensis</i>. The prevalence of <i>I. hookeri</i> in nymphs varied between 0% and 16% and was positively correlated with the encounter probability of ungulates and the densities of all life stages of <i>I. ricinus</i>. Lastly, we investigated the emergence of <i>I. hookeri</i> from artificially fed, field-collected nymphs. Adult wasps emerged from seven of the 172 fed nymphs. From these observations, we inferred that <i>I. hookeri</i> is parasitizing <i>I. ricinus</i> larvae that are feeding on deer, rather than on rodents or in the vegetation. Since <i>I. hookeri</i> populations depend on deer abundance, the main propagation host of <i>I. ricinus</i>, these wasps have no apparent effect on tick populations. The presence of <i>I. hookeri</i> may directly interfere with the transmission cycle of <i>A. phagocytophilum</i>, but not with that of <i>B. afzelii</i> or <i>N. mikurensis</i>.