The mitochondrial genome and the expression of the genes within it have evolved to be highly unusual in several lineages. Within alveolates, apicomplexans and dinoflagellates share the most reduced mitochondrial gene content on record, but differ from one another in organisation and function. To clarify how these characteristics originated, we examined mitochondrial genome form and expression in a key lineage that arose close to the divergence of apicomplexans and dinoflagellates, Oxyrrhis marina. We show that Oxyrrhis is a basal member of the dinoflagellate lineage whose mitochondrial genome has some unique characteristics while sharing others with apicomplexans or dinoflagellates. Specifically, Oxyrrhis has the smallest gene complement known, with several rRNA fragments and only two protein coding genes, cox1 and a cob-cox3 fusion. The genome appears to be highly fragmented, like that of dinoflagellates, but genes are frequently arranged as tandem copies, reminiscent of the repeating nature of the Plasmodium genome. In dinoflagellates and Oxyrrhis, genes are found in many arrangements, but the Oxyrrhis genome appears to be more structured, since neighbouring genes or gene fragments are invariably the same: cox1 and the cob-cox3 fusion were never found on the same genomic fragment. Analysing hundreds of cDNAs for both genes and circularized mRNAs from cob-cox3 showed that neither uses canonical start or stop codons, although a UAA terminator is created in the cob-cox3 fusion mRNA by post-transcriptional oligoadenylation. mRNAs from both genes also use a novel 5' oligo(U) cap. Extensive RNA editing is characteristic of dinoflagellates, but we find no editing in Oxyrrhis. Overall, the combination of characteristics found in the Oxyrrhis genome allows us to plot the sequence of many events that led to the extreme organisation of apicomplexan and dinoflalgellate mitochondrial genomes.