The APETALA2 (AP2) subfamily of transcription factors are key regulators of angiosperm root, shoot, flower, and embryo development. The broad diversity of anatomical and morphological structures is potentially associated with the genomic dynamics of the AP2 subfamily. However, a comprehensive phylogenomic analysis of the AP2 subfamily across angiosperms is lacking. We combined phylogenetic and synteny analysis of distinct AP2 subclades in the completed genomes of 107 angiosperm species. We identified major changes in copy number variation and genomic context within subclades across lineages, and discuss how these changes may have contributed to the evolution of lineage‐specific traits. Multiple AP2 subclades show highly conserved patterns of copy number and synteny across angiosperms, while others are more dynamic and show distinct lineage‐specific patterns. As examples of lineage‐specific morphological divergence due to AP2 subclade dynamics, we hypothesise that that loss of PLETHORA1/2 in monocots correlates with the absence of taproots, whereas independent lineage‐specific changes of PLETHORA4 /BABY BOOM and WRINKLED1 genes in Brassicaceae and monocots point towards regulatory divergence of embryogenesis between these lineages. Additionally, copy number expansion of TOE1 and TOE3/AP2 in asterids is implicated with differential regulation of flower development. Moreover, we show that the genomic context of AP2 s is in general highly specialised per angiosperm lineage. Our study is the first to shed light on the evolutionary divergence of the AP2 subfamily subclades across major angiosperm lineages and emphasises the need for lineage‐specific characterisation of developmental networks to further understand trait variability.