Bird pollination in Asia is regarded as an uncommon phenomenon and, therefore, only a few investigations on mating pattern and paternity in fruits of Asian bird-pollinated plants have been conducted. Here, we examined spatial genetic structure, pollen dispersal, and multiple paternity in a natural population of Bombax ceiba (B. ceiba) (Malvaceae) in Hainan Island, South China, using simple sequence repeat (SSR) markers. A low genetic diversity (He = 0.351 ± 0.0341 and 0.389 ± 0.043, respectively, for adults and offspring) and bottleneck effects were observed. Genetic kinship was significant within 400 m or in 1,800–3,800 m. Both the mating pattern and paternity analysis confirmed obligate xenogamy and a low multiple paternity in B. ceiba. There was a strongly negative relationship between the frequency of matings and the distance between mating pairs. The average pollen dispersal distance was 202.89 ± 41.01 m (mean ± SE) and the farthest distance of > 1 km was recorded. Realized mating events showed an extremely leptokurtic distribution within 1,200 m, suggesting that the pollen dispersal distance was consistent with the optimal foraging theory of generalist birds such as Zosterops spp. and Pycnonotus spp. Paternity per tree ranged from two to six and the average effective number of pollen donors per maternal plant was 3.773, suggesting a low level of paternity diversity as compared to other bird-pollinated plants. We concluded that optimal foraging behavior by generalist birds could explain the leptokurtic pollen dispersal distribution and predominantly near-neighbor matings in B. ceiba. The limited pollen dispersal distance and low multiple paternity were consistent with low fruit setting rate (3.27 ± 0.93%) in this self-incompatible tree, which was caused mainly by the restricted flight distance of birds and human disturbances. Low genetic diversity and significant spatial genetic structure might have largely resulted from logging and human collection of fruits.