Arthropod-borne viruses (arboviruses) are zoonotic agents with enzootic transmission cycles infecting people via direct spillover. Some arboviruses increase circulation by exploiting domesticated animals to increase human exposure, and a few can initiate and in some cases sustain transmission among human amplification hosts, typically transmitted by Aedes aegypti and sometimes other Aedes (Stegomyia) spp. mosquitoes. These include dengue, yellow fever and chikungunya viruses with histories of emergence into human-amplified epidemic cycles for centuries, infect millions of persons and spreading pandemically. More recently, the emergence and rapid spread of Zika virus in tropical regions of the South Pacific and Western Hemisphere took most arbovirologists and public health officials by complete surprise. This Zika emergence raised questions regarding our ability to identify other viruses with this potential for urbanization so that interventions can be developed proactively. The ecology, evolution and transmission of the enzootic ancestors of these urban arboviruses will be reviewed, along with factors that may promote or limit their emergence.