Plasmids of the incompatibility group IncP-1 can transfer and replicate in many genera of the Proteobacteria. They are composed of backbone genes that encode a variety of essential functions as well as accessory genes that have implications for human health and environmental remediation. While it is well understood that the accessory genes are transferred horizontally between plasmids, recent studies have also provided examples of recombination in the backbone genes of IncP-1 plasmids. As a consequence, phylogeny estimation based on backbone genes is expected to produce conflicting gene tree topologies. The main goal of this study was therefore to infer the evolutionary history of IncP-1 plasmids in the presence of both vertical and horizontal gene transfer. This was achieved by quantifying the incongruence among gene trees and attributing it to known causes such as, a) phylogenetic uncertainty, b) coalescent stochasticity, and c) horizontal inheritance. Topologies of gene trees exhibited more incongruence than could be attributed to phylogenetic uncertainty alone. Species-tree estimation using a Bayesian framework that takes coalescent stochasticity into account was well supported, but it differed slightly from the maximum likelihood tree estimated by concatenation of backbone genes. After removal of the gene that demonstrated a signal of intergroup recombination, the concatenated tree was congruent with the species-tree estimate, which itself was robust to inclusion/exclusion of the recombinant gene. Thus, in spite of horizontal gene exchange both within and among IncP-1 subgroups, the backbone genome of these IncP-1 plasmids retains a detectable vertical evolutionary history.