The trihelix transcription factor (TTF) gene family is an important class of transcription factors that play key roles in regulating developmental processes and responding to various stresses. To date, no comprehensive analysis of the TTF gene family in large-scale species has been performed. A cross-genome exploration of its origin, copy number variation, and expression pattern in plants is also unavailable. Here, we identified and characterized the TTF gene family in 110 species representing typical plant phylogenetic taxa. Interestingly, we found that the number of TTF genes was significantly expanded in Chara braunii compared to other species. Based on the available plant genomic datasets, our comparative analysis suggested that the TTF gene family likely originated from the GT-1-1 group and then expanded to form other groups through duplication or deletion of some domains. We found evidence that whole-genome duplication/triplication contributed most to the expansion of the TTF gene family in dicots, monocots and basal angiosperms. In contrast, dispersed and proximal duplications contributed to the expansion of the TTF gene family in algae and bryophyta. The expression patterns of TTF genes and their upstream and downstream genes in different treatments showed a functional divergence of TTF-related genes. Furthermore, we constructed the interaction network between TTF genes and the corresponding upstream and downstream genes, providing a blueprint for their regulatory pathways. This study provided a cross-genome comparative analysis of TTF genes in 110 species, which contributed to understanding their copy number expansion and evolutionary footprint in plants.