One of the defining events in Earth’s history is the origin of the flower, a highly compacted branch composed of modified leaves specialized for plant reproduction. The flower is the most complex plant structure and consists of elaborate organs, which have diversified tremendously in the extant ~350,000 species of flowering plants. Recent advances have provided considerable insight into the genetic basis of floral organ identity and diversification during plant evolution. Less understood remain the diversity of floral cell types and the genetic programs underlying cell type specification and divergence among species. Building upon Tabula Floris, our single-cell floral atlas of Arabidopsis thaliana, we have generated comparable developmental floral atlases for several related species in the mustard family (Brassicaceae), which span 25 million years of evolution, and have characterized the expression profiles of diverse floral cell populations. Using multispecies embedding based on orthologous genes, we have identified homologous floral cell types and inferred gene co-expression networks underlying their specialized functions and developmental programs. We have compared these networks to uncover shared nodes and modules, as well as identify unique network motifs, which may underlie phenotypic divergences. We further focus on the nectary secretory cell to study the contributions of phylogenetic distance and drift to homologous cell types with conserved function among species. By identifying transcriptionally co-expressed modules and mapping their distribution on a phylogenetic cell type tree, we have reconstructed the putative evolutionary steps which led to the origin of this highly specialized cell type and identified putative ancestral cell types. Our results outline a model for the origin and diversification of plant cell types through the specialization of the transcriptional programs and their deployment in different organ and developmental contexts of the flower.