Handroanthus chrysotrichus shows pollination-dependent self-fertility, polyploidy, and adventitious polyembryony, and it is closely related to H. ochraceus, for which apparently conflicting reports of self-incompatibility and apomixis have been published. The present study aims to investigate the polyembryony in these species by means of histological analysis of ovule/seed development in unpollinated, selfed, and crossed pistils/fruits (in H. chrysotrichus only) as well as seed germination experiments. Experimental pollinations were carried out to evaluate breeding systems in the studied populations, and the results indicated self-fertility in both species. Adventitious embryo precursor cells (AEPs) were formed in the ovules of unpollinated, selfed, and crossed pistils. However, unfertilized ovules never develop into seeds, and fertilization/endosperm initiation clearly stimulates the formation of AEPs in pollinated pistils. The inability of AEP-bearing unfertilized ovules to initiate endospermogenesis clearly shows that fertilization is needed for adventitious embryo development. Consequently, formation of AEPs is required but is not sufficient for apomictic reproduction in H. chrysotrichus. Analysis of the positions of multiple embryos in the endosperm indicated that fertilized ovules are able to develop into seeds even in the absence of a zygotic embryo. The development of AEPs in ovules of H. chrysotrichus foregoes the stage in which activation of selfed pistil rejection takes place in H. impetiginosus, a species with late-acting self-incompatibility. Our study supports the hypothesis that the self-fertility in H. chrysotrichus (and perhaps also in H. ochraceus) resulted from the emergence of pseudogamous apomixis, favored by the physiological peculiarities of the late-acting self-incompatibility and possibly related to polyploidy.