Tetrahymena thermophila, a classic ciliate model organism, has been shown to possess tubular mitochondrial cristae and highly divergent electron transport chain involving four transmembrane protein complexes (I–IV). Here we report cryo-EM structures of its ~8 MDa megacomplex IV2+ (I + III2+ II)2, as well as a ~ 10.6 MDa megacomplex (IV2+ I + III2+ II)2at lower resolution. In megacomplex IV2+ (I + III2+ II)2, each CIV2protomer associates one copy of supercomplex I + III2and one copy of CII, forming a half ring-shaped architecture that adapts to the membrane curvature of mitochondrial cristae. Megacomplex (IV2+ I + III2+ II)2defines the relative position between neighbouring half rings and maintains the proximity between CIV2and CIII2cytochromecbinding sites. Our findings expand the current understanding of divergence in eukaryotic electron transport chain organization and how it is related to mitochondrial morphology.