Chromatin remodeling complexes dynamically modify DNA accessibility to mediate changes in gene expression during eukaryotic cell cycle progression, developmental transitions, and environmental adaptation. Higher eukaryotes have multiple remodeler subtypes based on the incorporation of different ATPases; however, the coordination and functional specificity of these diverse complexes is not well understood. Apicomplexan parasites such as Toxoplasma gondii have a limited set of chromatin remodelers offering a divergent setting in which to explore the function of homologous complexes. These parasites have selectively retained the Myb domain–containing proteins with homology to chromatin-associated regulators like SNF2h and SWI3. Here, a comprehensive analysis of the Myb protein family in Toxoplasma defines the composition of two SWI3 complexes with mutually exclusive ATPase homologous—TgSNF2a and TgSNF2b. Integrating transcriptomics with a custom chromatin-profiling strategy, we show that TgSNF2a is essential for the timely transcription of genes, while TgSNF2b ensures global transcriptional competency and fidelity throughout the cell cycle and developmental transitions. Cell cycle–resolved chromatin profiling conclusively shows the shift from TgSNF2b to TgSNF2a occupancy when regulated genes transition from being poised to being actively transcribed. Our findings demonstrate that TgSNF2a and TgSNF2b perform distinct yet interdependent regulatory roles shaped by their chromatin context. This work uncovers ancestral principles of chromatin regulation and offers new insight into the functional diversification of SWI/SNF complexes across eukaryotes.