In this paper, we examine the diversity and character transformation in pollen morphology and ultrastructure (of the pollen wall and aperture system) of the tribe Chelidonieae, the only Papaveraceae group including anemophilous species. Representatives of the nine Chelidonieae genera and three external species were studied using light, scanning-electron, and transmission-electron microscopy. A recently published phylogenetic hypothesis of Chelidonieae was used as a framework to infer the plesiomorphic character states of the tribe and to trace the evolutionary trends of pollen features, using parsimony optimisation. Chelidonieae pollen is generally medium-sized, spheroidal, microechinate-microreticulate, with a granular aperture membrane, an exine stratified in a discontinuous tectum with irregular internal face, a columellar infratectum, and foot layer, with endexine, and a uni-layer intine. Variation among taxa results mainly from: the apertural system (varying in the shape [colpi, pores]; the number [3–12] and position [zono-, panto-aperturate] of the apertures); wall ornamentation (with three more types in addition to the general type); the thickness of the layers of the interapertural exine; and, at the apertural level, the presence or not of endoapertures, and the structure of the foot layer. We have detected a general variation pattern in the thickness of the exine layers consisting of an inverse relationship between their proportions (ectexine vs. endexine, and tectum vs. infratectum). Similarly, the great development of endexine in Sanguinaria appears to have been favoured by the lack of a foot layer in the ectexine. We have found endoapertures in Bocconia pollen, which is the first report in Papaveraceae and represents the most basal lineage of Eudicots in which endoapertures have been detected. We describe for first time in angiosperms a thickening of the foot layer at the apertural level, in Bocconia and Macleaya, with a digit-shaped disruption around the pore (with white lines inside during microspore), that we call a “digit-shaped structure” and we relate to the harmomegathy process. We have inferred the plesiomorphic character states of Chelidonieae pollen and have identified 48 transformations. The evolutionary trend in the apertural system of Chelidonieae goes from many pore-shaped apertures arranged globally (pantoporate) to pollens with three equatorial colpi, contrary to the general trend in angiosperm pollen. Most of the variations in the characters occurred independently in the current taxa lineages and only 11 changes are synapomorphies supporting Chelidonieae groupings. The colpate Chelidonieae clade is supported by two character-state transitions, but no synapomorphy supports the molecular relationship of Bocconia and Macleaya with the colpate clade. According to our results, a strong pollen transformation occurred in the Bocconia-Macleaya lineage, with five of the 11 synapomorphies identified. We discuss this pollen transformation in relation to the shift in the pollination system, from zoophily to anemophily, which occurred in this Chelidonieae lineage.