Mitochondria are essential components of eukaryotic cells. They possess their own gene expression machineries where highly divergent and specialized ribosomes, named hereafter mitoribosomes, translate the few, although essential, mitochondrial messenger RNAs still encoded by mitochondrial genomes. Here, we present the biochemical and structural characterization of the model green alga Chlamydomonas reinhardtii mitoribosome as well as the functional study of some of its Chlamydomonas specific components. We provide a single particle cryo-electron microscopy structure of Chlamydomonas mitoribosome and show how its core is composed by the assembly of 13 rRNA fragments encoded by separate non-contiguous gene pieces. While 5S rRNA was assumed to be absent from Chlamydomonas mitoribosome, a small rRNA representing a highly divergent 5S rRNA occurs in its central protuberance. In contrast, a gene piece that was believed to encode a fragment of rRNA encodes a small RNA that does not occur in the mitoribosome. Eleven novel proteins, mainly helical repeat proteins, including OPR, PPR and mTERF proteins occur in Chlamydomonas mitoribosome, revealing in particular the first structure of an OPR protein in complex with its RNA target. Reverse genetic studies reveal that the functions of some of the novel helical repeat proteins are required for mitoribosome biogenesis. The long studied p32 protein, whose function was related to several mitochondrial diseases in Human uniquely occurs as a constitutive ribosomal protein in the small subunit. Finally, cryo-electron tomography and biochemical studies show that Chlamydomonas mitoribosomes are exclusively attached to the mitochondrial inner membrane via two contact points mediated by Chlamydomonas specific novel proteins. One of them provides a direct interface between the exit of the peptide channel and the insertase Oxa1 for the insertion of nascent proteins in the mitochondrial inner membrane.