Arthropod-borne viruses (arboviruses) are maintained in nature by cycling between vertebrate hosts and haematophagous invertebrate vectors. These viruses are responsible for causing a significant public health burden throughout the world, with over 100 species having the capacity to cause human disease. Arbovirus outbreaks in previously naïve environments demonstrate the potential of these pathogens for expansion and emergence, possibly exacerbated more recently by changing climates. These recent outbreaks, together with the continued devastation caused by endemic viruses, such as Dengue virus which persists in many areas, demonstrate the need to better understand the selective pressures that shape arbovirus evolution. Specifically, a comprehensive understanding of host-virus interactions and how they shape both host-specific and virus‑specific evolutionary pressures is needed to fully evaluate the factors that govern the potential for host shifts and geographic expansions. One approach to advance our understanding of the factors influencing arbovirus evolution in nature is the use of experimental studies in the laboratory. Here, we review the contributions that laboratory passage and experimental infection studies have made to the field of arbovirus adaptation and evolution, and how these studies contribute to the overall field of arbovirus evolution. In particular, this review focuses on the areas of evolutionary constraints and mutant swarm dynamics; how experimental results compare to theoretical predictions; the importance of arbovirus ecology in shaping viral swarms; and how current knowledge should guide future questions relevant to understanding arbovirus evolution.