An accurate phylogeny of animals is needed to clarify their evolution, ecology, and impact on shaping the biosphere. Although multi-gene alignments of up to several hundred thousand amino acids are nowadays routinely used to test hypotheses of animal relationships, some nodes towards the root of the animal phylogeny are proving hard to resolve. While the relationships of the non-bilaterian lineages, primarily sponges (Porifera) and comb jellies (Ctenophora), have received much attention since more than a decade, controversies about the phylogenetic position of the worm-like bilaterian lineage Xenacoelomorpha and the monophyly of the “Superphylum” Deuterostomia have more recently emerged. Here we independently analyse novel genome gene content and morphological datasets to assess patterns of phylogenetic congruence with previous amino-acid derived phylogenetic hypotheses. Using statistical hypothesis testing, we show that both our datasets very strongly support sponges as the sister group of all the other animals, Xenoacoelomorpha as the sister group of the other Bilateria, and largely support monophyletic Deuterostomia. Based on these results, we conclude that the last common animal ancestor may have been a simple, filter-feeding organism without a nervous system and muscles, while the last common ancestor of Bilateria might have been a small, acoelomate-like worm without a through gut.