The taxonomy of the subfamily Linoideae at the intergeneric and section levels has been questioned throughout the years, and the evolution of floral characters remains poorly understood. In particular, the evolution of flower color is still uncertain, despite its ecological importance and being one of the most variable and striking traits in Angiospermae. We evaluated the phylogenetic relationships of the genera and sections and used the phylogeny to reconstruct the ancestral state of flower color. The results suggest reevaluating the taxonomic status of segregated genera and re-incorporating them into Linum. Four of the five sections currently accepted were recovered as monophyletic (Cathartolinum, Dasylinum, Linum, and Syllinum). We propose accepting the section Stellerolinon and reevaluating Linopsis, whose representatives were recovered in three separate clades. The ancestral flower color for Linoideae was yellow-white. The flower colors purple and yellow-white were recovered at the deepest nodes of the two main clades. Pink, blue, and red colors were the most recent to evolve. These results appear to be related to diversification events, biogeographical history, and ecological aspects of the subfamily. Our reconstruction constitutes the first plausible scenario that explores the evolution of flower color, leading to new testable hypotheses for future research on the flax group.