The Apicomplexa phylum is composed entirely of obligate intracellular parasites. Among them, Toxoplasma gondii is both a prominent pathogen, causative agent of toxoplasmosis, and a model organism. A peculiar feature shared by most apicomplexans is the presence of two distinct DNA-containing organelles of endosymbiotic origin: the mitochondrion and the apicoplast. Particular attributes of these organelles, including their morphology, ultrastructure, and segregation processes, underpinned by their bacterial origins, represent attractive targets for antiparasitic drug development due to their divergence from mammalian host cells. They showcase several peculiarities. One of them is their significant genomic reductions, characteristics likely associated with adaptations to their ecological niches. Despite minimized genomes, they retain essential bacterial-like translation mechanisms and have evolved sophisticated protein import systems to maintain critical functions. Recent breakthroughs in long-read sequencing technologies have provided invaluable insights into the complexity of coccidian mitogenomes, especially the T. gondii mitochondrial genome. This genome is characterized by a specific arrangement of sequence blocks that encode essential components for the electron transport chain. However, the complete architecture of the mitochondrial genome remains elusive, including the presence of potentially multiple mitochondrial genomes within a single individual and whether post-transcriptional processing occurs or not. The apicoplast—a relic of a red algal endosymbiont—underscores the evolutionary trajectory of T. gondii, with its anabolic ability to sustain vital metabolic pathways. Despite its compact size and low GC content, the apicoplast genome presents a conserved structure across species. Furthermore, the coordination of organelle dynamics with nuclear DNA replication reveals the deep interplay between endosymbionts and the life cycle of T. gondii, demonstrating a delicate balance between evolutionary conservation and innovation. Further understanding the role of these divergent organelles and the essential genes they encode in the process of adaptation to parasitism will open new opportunities for therapeutic interventions directed against the core biological processes of apicomplexan parasites.