‘Oligotrichous’ ciliates have been traditionally placed in a presumed monophyletic taxon called the Oligotrichia. However, gene sequences of the small subunit rRNA gene, and several other genes, suggest that the taxon is not monophyletic: although statistical support for this is not strong, the oligotrich Halteria grandinella is associated with the hypotrich ciliates and not with other oligotrich genera, such as Strombidium and Strombidinopsis. This has convinced some taxonomists to emphasize that morphological features strongly support the monophyly of the oligotrichs. To further test this hypothesis of monophyly, we have undertaken a phylogenomic analysis using the transcriptome of H. grandinella cells amplified by a single-cell technique. One hundred and twenty-six of 159 single-gene trees placed H. grandinella as sister to hypotrich species, and phylogenomic analyses based on a subset of 124 genes robustly rejected the monophyly of the Oligotrichia and placed the genus Halteria as sister to the hypotrich genera Stylonychia and Oxytricha. We use these phylogenomic analyses to assess the convergent nature of morphological features of oligotrichous ciliates. A particularly ‘strong’ morphological feature supporting monophyly of the oligotrichs is enantiotropic cell division, which our results suggest is nevertheless a convergent feature, arising through the need for dividing ciliates to undertake rotokinesis to complete cell division.