The classification of the Thaumatopsyllidae within the Copepoda has been an issue of ongoing discussion since the discovery of Thaumatopsyllus paradoxus G.O. Sars, 1913 from the Norwegian coast. The family has been formally placed in the Monstrilloida, the Cyclopoida and even in its own order, the Thaumatopsylloida, based on different morphological criteria. We examined for the first time, the phylogenetic position of the Thaumatopsyllidae using gene sequences of 28S and 18S rRNA, as well as COI mtDNA, obtained from two thaumatopsyllid species occurring off the coast of southern California. We also fortuitously explored the phylogenetic relationships of the Cyclopoida in more detail than Khodami et al. (2017) by including a wider sample of key families such as the Erebonasteridae and Gisellinidae. Both Maximum Likelihood and Bayesian analyses revealed the Thaumatopsyllidae is nested in the Cyclopoida and is related to the marine Speleoithonidae. In addition, 16 families of the Cyclopoida are supported to be monophyletic, but surprisingly, the Cyclopidae is paraphyletic. The Cyclopicinidae is the first monophyletic offshoot of the cyclopoid tree, followed by two derived clades. The first clade contains a monophylum consisting of the Schminkepinellidae + Giselinidae which is sister to a clade including the monophyletic Erebonasteridae and all other poecilostome families. The second clade is divided into two main, well-supported family clusters. One includes the Cyclopidae encompassing two subfamilies (Eucylopinae and Cyclopinae), but unexpectedly the parasitic Lernaeidae cluster as a sister-group to the brackish water Halicyclops (subfamily Halicyclopinae) and the Euryteinae is the sister to all the rest of Cyclopidae s. l., making the Cyclopidae paraphyletic. To resolve this conundrum, we erected two families, Euryteidae and Halicyclopidae. The Cyclopidae s. str. retains the subfamilies Eucyclopinae and Cyclopinae, although our phylogeny does not support the reciprocal monophyly of these subfamilies. Our results support the gradual invasion of fresh water by the four families in this cluster. The highly supported monophyletic marine Euryteidae is the first offshoot followed by the brackish-water, free-living Halicyclopidae and the freshwater, parasitic Lernaeidae. The Cyclopidae fulfilled the colonization of freshwater bodies. The other clade of families comprises 12 monophyletic families recovered by our analysis, including the Pterinopsyllidae (at first offshoot), the Smirnovipinidae sister to the Hemicyclopinidae + Psammocyclopinidae, the Thaumatopsyllidae + Speleoithonidae, an undescribed family sister to the Archinotodelphyidae + Notodelphyidae and the Cyclopinidae sister to the Oithonidae + Cyclopettidae. We propose suborder ranks for each of the four main phylogenetic subdivisions of the Cyclopoida. These are named Cyclopicinida, Ergasilida, Cyclopida and Oithonida after the type genus of the oldest described family in the respective group.