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Cnidarians are critical members of aquatic communities and have been an experimental system for a diversity of research areas ranging from development to biomechanics to global change biology. Yet, we still lack a well-resolved, taxonomically balanced cnidarian tree of life to place this research in appropriate phylogenetic context. To move towards this goal, we combined data from 26 new anthozoan transcriptomes with 86 previously published cnidarian and outgroup datasets to generate two 748-locus alignments containing 123,051 (trimmed) and 449,935 (untrimmed) amino acids. We estimated maximum likelihood phylogenies for both matrices under partitioned and unpartitioned site-homogeneous and site-heterogenous models of substitution. We used the resulting topology to constrain a phylogenetic analysis of 1,814 small subunit ribosomal (18S) gene sequences from GenBank. Our results confirm the position of Ceriantharia (tube-dwelling anemones), a historically recalcitrant group, as sister to the rest of Hexacorallia across all phylogenies regardless of data matrix or model choice. We find unanimous support for the sister relationships of Scleractinia and Corallimorpharia and of Endocnidozoa and Medusozoa. We propose the name Coralliformes for the clade uniting scleractinians and corallimorpharians and the name Operculozoa for the clade uniting endocnidozoans and medusozoans. Of the 229 genera with more than a single representative in our 18S hybrid phylogeny, 47 (21%) were identified as monophyletic, providing a starting point for a number of taxonomic revisions. Together, these data are an invaluable resource for comparative cnidarian research and provide perspective to guide future refinement of cnidarian systematics.