The order Holosporales is a broad and ancient lineage of bacteria obligatorily associated with eukaryotic hosts, mostly protists. Significantly, this is similar to other evolutionary distinct bacterial lineages (e.g. Rickettsiales and Chlamydiae). Here, we provide a detailed and comprehensive account on the current knowledge on the Holosporales. First, acknowledging the up-to-date phylogenetic reconstructions and recent nomenclatural proposals, we reevaluate their taxonomy, thus re-ranking them as a suborder, i.e. Holosporineae, within the order Rhodospirillales. Then, we examine the phylogenetic diversity of the Holosporineae, presenting the 20 described genera and many yet undescribed sub-lineages, as well as the variety of the respective environments of provenance and hosts, which belong to several different eukaryotic supergroups. Noteworthy representatives of the Holosporineae are the infectious intranuclear Holospora, the host manipulator 'Caedimonas', and the farmed shrimp pathogen 'Candidatus Hepatobacter'. Next, we put these bacteria in the broad context of the whole Holosporineae, by comparing with the available data on the least studied representatives, including genome sequences. Accordingly, we reason on the most probable evolutionary trajectories for host interactions, host specificity, and emergence of potential pathogens in aquaculture and possibly humans, as well as on future research directions to investigate those many open points on the Holosporineae.