Dengue is a prevalent disease in Colombia and all dengue virus serotypes (DENV-1 to -4) co-circulate in the country since 2001. However, the relative impact of gene flow and local diversification on epidemic dynamics is unknown due to heterogeneous sampling and lack of sufficient genetic data. The region of Santander is one of the areas with the highest incidence of dengue in Colombia. To provide a better understanding of the epidemiology of dengue, we inferred DENV population dynamics using samples collected between 1998 and 2015. We used Bayesian phylogenetic analysis and included 143 new envelope gene sequences from Colombia, mainly from the region of Santander, and 235 published sequences from representative countries in the Americas. We documented one single genotype for each serotype but multiple introductions. Whereas the majority of DENV-1, DENV-2, and DENV-4 strains fell into one single lineage, DENV-3 strains fell into two distinct lineages that co-circulated. The inferred times to the most recent common ancestors for the most recent clades of DENV-1, DENV-2, and DENV-4 fell between 1977 and 1987, and for DENV-3 was around 1995. Demographic reconstructions suggested a gradual increase in viral diversity over time. A phylogeographical analysis underscored that Colombia mainly receives viral lineages and a significant diffusion route between Colombia and Venezuela. Our findings contribute to a better understanding of the viral diversity and dengue epidemiology in Colombia.