Protein-protein interactions are central to the regulation and function of transcription factors in time- and cell-specific regulation of the genome. Increases in interactome complexity may serve as a mechanistic driver for evolutionary novelty. This novelty could arise as temporal and spatial gene expression becomes differentially regulated. Here, we used a combinatory phylogenetic and algorithmic approach to characterize the diversification of interactomes for the bZIP family across 18 metazoans and three unicellular outgroups. Our bZIP gene tree analyses identified two new subfamilies (CREBL2 and CREBZF) across animals and reinforce previous bZIP family classifications, indicating that diversification occurred in two waves, prior to the animal ancestor (12 of 18 subfamilies) and then again after the cnidarian-bilaterian ancestor (6 of 18 subfamilies). Expansions and losses of bZIP subfamilies with different dimerization capacities drive substantial variations in interactomes of ctenophores, placozoans, cnidarians, and vertebrates. While these expansions and losses result in a large majority of the observed rewiring of the metazoan interactome, variability of per transcription factor connectedness itself was also a factor, with total dimers shifting by two-fold while bZIP count remains consistent between invertebrate bilaterians. Heterodimeric potential for particular bZIP orthologs spanning more than 1 billion years, suggesting an evolutionary constraint on protein-protein interactions. Collectively, the interactome connectedness for bZIP transcription factors has undergone large and uneven changes across animal evolution driven principally by gene duplication and loss, and changes in the interaction behavior of the proteins themselves plays a less significant but impactful role