Benthesicymidae is a monophyletic group of Decapoda adapted to a life on the sea-floor, in the near-bottom layer, in the bathy- and in the mesopelagic, within an impressive depth range from a few hundred metres (Gennadas) to several thousand metres (Benthesicymus). Higher taxa are known to conquer all main oceanic biotopes such as the benthic, benthopelagic, and pelagic and a wide depth range but few family-level groups have clades evolved within all these oceanic realms. Therefore, the global fauna of Benthesicymidae provides a rare opportunity for an insight into phylogenetic processes favouring colonisation of all principal oceanic biotopes. The first comprehensive phylogenetic study of Benthesicymidae (all 37 valid species) is based on six molecular markers and 105 morphological characters (including 72 female and male copulatory characters). Analyses resulted in trees with similar topology and the same set of robust clades. Molecular methods based on 167 sequences (84 new) provided better resolution of deeper nodes and generally higher support of the clades, while morphological methods allowed analyses of all valid species of the global fauna. Phylogenetic analyses support the monophyly and robustness of all currently known genera except Gennadas, which was split into Gennadas Bate, 1881, Amalopenaeus Smith, 1882, and Notogennema gen. nov. We also retrieved two major clades for which we erected two new subfamilies: Benthesicyminae subfam. nov. (presumably benthic, genera Altelatipes, Bathicaris, Benthesicymus, and Benthonectes) and Gennadinae subfam. nov. (presumably pelagic, genera Amalopenaeus, Bentheogennema, Benthoecetes, Boreogennema, Gennadas, Maorrancaris, and Notogennema gen. nov.). We revealed two groups of morphological characters, that are interlinked evolutionarily: (1) petasma and thelycum; (2) body, mouthparts, and pereopods. Morphological traits within benthic and pelagic clades are different, a model explaining the differences is proposed. Along with previous studies, our results confirm the idea that the elaboration of the copulatory structures is a key to successful colonisation of the pelagic realm. These results extend our knowledge about evolution in the largest habitual biotope of our planet and phylogenetic processes favouring colonisation of all principal oceanic biotopes.