The pinewood nematode (Bursaphelenchus xylophilus) is known to be the causative agent of pine wilt disease, which is transmitted from wilt-killed to healthy pine trees by the insect vector Monochamus alternatus. The second-stage propagative juvenile develops into third-stage dispersal (JIII) or propagative juveniles. The JIII develops into the fourth-stage dispersal juvenile (JIV), a special stage for transportation, then the JIV enters the tracheal system of adult beetles in pupal chambers in the xylem. To determine the differences in some life history parameters related to transmission between a virulent and an avirulent isolate of B. xylophilus, progression to the different life stages was investigated using two nematode isolates of different virulence, M. alternatus larvae, and pine bolts with an artificial pupal chamber. The numbers of JIIIs and JIVs produced around the pupal chamber by the time of beetle emergence were much smaller in the avirulent isolate than in the virulent one. The proportion of JIIIs produced in a population around the pupal chamber (the JIII and JIV number/the total population) and the probability of JIIIs developing into JIVs (the JIV number/the JIII and JIV number) were also smaller in the avirulent isolate. Although the probability of JIVs boarding beetles (the initial nematode load/the JIV number) was equal between the two isolates, the mean initial nematode load was much smaller in the avirulent isolate. The smaller initial nematode load of the avirulent isolate was ascribed to its smaller rate of reproduction and to lower production rates of JIII and JIV. A trade-off between the virulence and transmission rate of B. xylophilus is discussed herein, taking into account the effect of the initial nematode load on the vector’s longevity and flight performance.