Aphelenchoides besseyi is an obligate parasite that often causes white-tip symptoms in rice plants. The nematode exhibits ectoparasitic behaviour with its infection rate matching the development of rice plants. Few studies have analysed how A. besseyi migration is influenced by chemical and host factors. Here, we focused on the effects of auxins on nematode migration and propagation. Exposure of A. besseyi to an auxin gradient created by a Pluronic F-127 gel resulted in nematode aggregation at the highest auxin concentration tested, 100 μm. Inoculation on the susceptible cv. Ningjing1 produced more nematodes than on the resistant rice cv. Tetep, which correlated with their endogenous auxin levels. Young panicles treated with 1-naphthaleneacetic acid produced more grains and nematodes, whereas plants treated with the auxin transport inhibitor, 2,3,5-triiodobenzoic acid, led to fewer nematodes in the seeds. In addition, A. besseyi rarely migrated and multiplied in the plants of the male sterile rice cv. Zhenshan97A, which had insufficient auxin level in pollen and thus could not generate any grains in most panicles. However, large numbers of nematodes were observed in seeds of cv. Zhenshan97A that had received pollens from the maintainer cv. Zhenshan97B. The results indicate that auxin might play a key role in the migration and propagation of A. besseyi.