After the merger of the former Taxodiaceae and Cupressaceae s.s., currently the conifer family Cupressaceae (sensu lato) comprises seven subfamilies and 32 genera, most of which are important components of temperate and mountainous forests. With the exception of a recently published genus-level phylogeny of gymnosperms inferred from sequence analysis of 790 orthologs, previous phylogenetic studies of Cupressaceae were based mainly on morphological characters or a few molecular markers, and did not completely resolve the intergeneric relationships. In this study, we reconstructed a robust and well-resolved phylogeny of Cupressaceae represented by all 32 genera, using 1944 genes (Orthogroups) generated from transcriptome sequencing. Reticulate evolution analyses detected a possible ancient hybridization that occurred between ancestors of two subclades of Cupressoideae, including Microbiota-Platycladus-Tetraclinis (MPT) and Juniperus-Cupressus-Hesperocyparis-Callitropsis-Xanthocyparis (JCHCX), although both concatenation and coalescent trees are highly supported. Moreover, divergence time estimation and ancestral area reconstruction indicate that Cupressaceae very likely originated in Asia in the Triassic, and geographic isolation caused by continental separation drove the vicariant evolution of the two subfamilies Cupressoideae and Callitroideae in the northern and southern hemispheres, respectively. Evolutionary analyses of some morphological characters suggest that helically arranged linear-acicular leaves and imbricate bract-scale complexes represent ancestral states, and the shift from linear-acicular leaves to scale-like leaves was associated with the shift from helical to decussate arrangement. Our study sheds new light on phylogeny and evolutionary history of Cupressaceae, and strongly suggests that both dichotomous phylogenetic and reticulate evolution analyses be conducted in phylogenomic studies.