Ceratozamia comprises 39 cycad species that occur throughout climatically varied montane habitats in Mesoamerica. To date, its species relationships and the ecological trends during its evolution remain unclear. We aimed to clarify the phylogenetic relationships, the timing of clade and species divergences, and the niche evolution throughout its phylogenetic history. Using genome-wide DNA sequences, an ultrametric species tree was constructed. Divergence times among branches and ancestral niches were estimated. The niche variation among species was evaluated, and their ancestral states were reconstructed to test whether niche shifts among branches can be explained by random processes. Ceratozamia comprises three main clades that have diversified since the Oligocene, with major divergence events occurring during the Miocene. This timing is consistent with fossil evidence, the timing estimated for other Neotropical plant groups, and the major geological events that shaped the topographic and climatic variation in Mexico. A Brownian Motion model explains little the niche evolution in the genus. Rather, non-random evolution via niche conservatism and niche divergence explain the diversification of Ceratozamia at lower and higher latitude ranges, respectively. We present the most comprehensive phylogenetic reconstruction for Ceratozamia and identify the environmental factors involved in the clade and species diversification.