The enigmatic and rare spiders of the family Deinopidae are known for their extremely large ocelli and their unique habit of casting their small cribellate webs over nocturnal pedestrian or aerial prey. Although the monophyly of the family has not been controversial, deinopid descriptive systematics has been neglected since the original species descriptions. The first goal of this monograph is to test the monophyly of Deinopidae and its genera and thus to establish a phylogenetically informed taxonomy of the species. We provide the first phylogeny of this family on the basis of 53 morphological and 3 behavioral characters scored for 17 deinopid species and 2 outgroups. Extant deinopid spiders belong to two genera: the larger pantropical Deinopis MacLeay, 1839, diagnosed by the extreme size of their posterior median eyes, and the smaller Menneus Simon, 1876, of the Old World (sub)tropics with normally sized eyes. Avella Pickard-Cambridge, 1877, and Avellopsis Purcell, 1904, are junior synonyms of Menneus as their type species are nested throughout Menneus phylogeny. The second goal is to revise the non-Deinopis species of Deinopidae. Here, we recognize, diagnose, illustrate, describe, and phylogenetically place the 14 known Menneus species. Africa currently has six species: Menneus camelus Pocock, 1902, from South Africa; M. capensis (Purcell, 1904) new combination from Western Cape, South Africa; M. darwini new species from Tanzania; M. dromedarius Purcell, 1904 (removed from synonymy of M. camelus), from South Africa and Madagascar; M. samperi new species from Kenya, Tanzania, and Uganda; and M. tetragnathoides Simon, 1876 (M. affinis Tullgren, 1910 new synonym), from Angola, Malawi, and Tanzania. Australasia currently has eight species: M. aussie new species from eastern Australia and New Caledonia; M. bituberculatus new species from Queensland and Indonesian West Papua; M. superciliosus (Thorell, 1881) from eastern Australia; M. nemesio new species from New South Wales; M. neocaledonicus (Simon, 1889) from New Caledonia, M. quasimodo new species from Western Australia; M. trinodosus Rainbow, 1920 (Deinopis insularis Rainbow, 1920, new synonym), from Queensland and New South Wales; and M. wa, new species, from Western Australia. We propose Avella angulata L. Koch, 1878, Avella despiciens O. P.-Cambridge, 1877, and Avella unifasciata L. Koch, 1878, as nomina dubia. Paleomicromenneus lebanensis Penney, 2003, the earliest known fossil, is similar to Menneus. Menneus is phylogenetically sister to Deinopis, and within Menneus we recover a grade of Australasian species that includes the African M. capensis, followed by a distal clade of African species with peculiar asymmetric somatic morphology.