Hybridization, incomplete lineage sorting, and phylogenetic error produce similar incongruence patterns, representing a great challenge for phylogenetic reconstruction. Here, we use sequence capture data and multiple species tree and species network approaches to resolve the backbone phylogeny of the Neotropical genus Lachemilla, while distinguishing among sources of incongruence. We used 396 nuclear loci and nearly complete plastome sequences from 27 species to clarify the relationships among the major groups of Lachemilla, and explored multiple sources of conflict between gene trees and species trees inferred with a plurality of approaches. All phylogenetic methods recovered the four major groups previously proposed for Lachemilla, but species tree methods recovered different topologies for relationships between these four clades. Species network analyses revealed that one major clade, Orbiculate, is likely of ancient hybrid origin, representing one of the main sources of incongruence among the species trees. Additionally, we found evidence for a potential whole genome duplication event shared by Lachemilla and allied genera. Lachemilla shows clear evidence of ancient and recent hybridization throughout the evolutionary history of the group. Also, we show the necessity to use phylogenetic network approaches that can simultaneously accommodate incomplete lineage sorting and gene flow when studying groups that show patterns of reticulation.