Background Viruses such as dengue virus (DENV), Zika virus (ZIKV), and chikungunya virus (CHIKV) pose major threats to human health, causing endemic, emerging, and reemerging diseases. These arboviruses have complex life cycles involving Aedes mosquitoes, driven by environmental, ecological, socioeconomic, and cultural factors. In Colombia, Aedes aegypti is the primary vector, but Aedes albopictus is expanding across the country. Understanding the unique characteristics of each species is crucial for managing arbovirus spread, particularly in areas where they coexist. Methodology/Principal Findings We conducted an entomological survey of A. aegypti and A. albopictus (larvae, pupae, and adults) in urban and rural areas of four municipalities across different elevations (200-2200 meters above sea level) in Colombia. Household conditions and knowledge of DENV were assessed through interviews. Female A. albopictus were tested individually for arbovirus RNA, while A. aegypti were tested in pools. Both species were found up to 2100 masl. A. aegypti comprised 78% of the immature forms collected, while A. albopictus made up 22%. Larvae from both species coexisted in common artificial breeding sites in urban and rural areas, with no evidence of competition. A. albopictus preferred rural areas, lower elevations (<1500 masl), high precipitation (>270 mm), and poor household conditions, while A. aegypti was more abundant in urban areas, intradomicile environments, and areas with moderate precipitation (100-400 mm). Biting risk was higher for A. aegypti (0.02-0.22 females per person), particularly in urban areas, while A. albopictus exhibited lower biting risk (0.001-0.08), with the highest values in rural Patia. Natural infections of DENV (12.4%) and CHIKV (12.4%) were found in A. aegypti, while A. albopictus showed CHIKV (41.2%) and DENV (23%) infections, with virus dissemination to the legs and salivary glands. Conclusions/Significance Integrating household conditions and community knowledge with environmental data can enhance predictive models for vector presence and guide surveillance and educational strategies. Our findings highlight the need to consider A. albopictus as a potentially significant arbovirus vector in Colombia, especially given the presence of arboviruses in its salivary glands, its use of artificial breeding sites, its biting risk inside homes, and its differing ecological preferences and seasonal associations compared to A. aegypti.