Elucidating relationships among early animal lineages has been difficult, and recent phylogenomic analyses place Ctenophora sister to all other extant animals, contrary to the traditional view of Porifera as the earliest-branching animal lineage. To date, phylogenetic support for either ctenophores or sponges as sister to other animals has been limited and inconsistent among studies. Lack of agreement among phylogenomic analyses using different data and methods obscures how complex traits, such as epithelia, neurons, and muscles evolved. A consensus view of animal evolution will not be accepted until datasets and methods converge on a single hypothesis of early metazoan relationships and putative sources of systematic error (e.g., long-branch attraction, compositional bias, poor model choice) are assessed. Here, we investigate possible causes of systematic error by expanding taxon sampling with eight novel transcriptomes, strictly enforcing orthology inference criteria, and progressively examining potential causes of systematic error while using both maximum-likelihood with robust data partitioning and Bayesian inference with a site-heterogeneous model. We identified ribosomal protein genes as possessing a conflicting signal compared with other genes, which caused some past studies to infer ctenophores and cnidarians as sister. Importantly, biases resulting from elevated compositional heterogeneity or elevated substitution rates are ruled out. Placement of ctenophores as sister to all other animals, and sponge monophyly, are strongly supported under multiple analyses, herein.