Phoretic mites of bark beetles are classic examples of commensal ectosymbionts. However, many such mites appear to have mutualisms with fungi that could themselves interact with beetles. We tested for indirect effects of phoretic mites on Dendroctonus frontalis, which attacks and kills pine trees in North America. Tarsonemus mites are known to carry ascospores of Ophiostoma minus, which tends to outcompete the mutualistic fungi carried by D. frontalis. Experimental additions and removals of mites from beetles demonstrated that Tarsonemus propagate O. minus in beetle oviposition galleries. Furthermore, the abundance of Tarsonemus and O. minus tended to covary in nature. These results verified a strong mutualism between Tarsonemus and O. minus. Results also indicated that O. minus is an antagonist of D. frontalis: beetle larvae seldom survived in the presence of O. minus (compared to 83% survival elsewhere). Apparently, this is an indirect result of O. minus outcompeting the two species of mycangial fungi that are critical to beetle nutrition. Thus, Tarsonemus mites close a loop of species interactions that includes a commensalism (mites and beetles), a mutualism (mites and O. minus), asymmetric competition (O. minus and mycangial fungi), and another mutualism (mycangial fungi and beetles). This interaction system produces negative feedback that could contribute to the endogenous population dynamics of D. frontalis. Reproductive rate of Tarsonemus was more temperature-sensitive than beetle generation time (which constrains the time for mite reproduction within a tree). This differential temperature sensitivity produces a narrow range of temperatures (centred at 27°C) in which mite reproduction per D. frontalis generation can attain its maximum of 100 mites/beetle. Consequently, seasonal oscillations in temperature are predicted to produce oscillations in the D. frontalis community, and climatic differences between regions could influence the community to dampen or exacerbate the cyclical outbreak dynamics of D. frontalis.