Orthotrichum and Ulota are two of the most speciose genera of the xerophytic moss family Orthotrichaceae. Here we reconstructed the phylogeny of these two genera using three data matrices: (1) organellar genomes and 33 taxa; (2) six loci from three genomes and 144 taxa; and (3) two plastid loci and 163 taxa. The present phylogeny, based on the maximum sampling of genes or taxa hitherto generally confirms the new classification of Orthotrichum and Ulota, and indicated that all Ulota species, except U. phyllantha, form a clade and three lineages comprising the cryptoporous Orthotrichum clade. We provided new morphological characters that support the present division of the two genera. Ancestral state reconstruction of stoma indicates that superficial stomata in Orthotrichum represent a plesiomorphic character and semi-immersed stomata were derived from immersed stomata. The results also suggest that immersed stomata independently arose once in Orthotrichum, whereas semi-immersed stomata probably arose more than once. Molecular dating analysis reveals that the occurrence of immersed stomata is probably related to arid environments during the early Oligocene to late Miocene, while the appearance of semi-immersed stomata may be associated with the mesic-xeric or semiarid environments during the middle Miocene to Pliocene. Ancestral state reconstruction of habitat indicates that the saxicolous habitat is apomorphic and independently evolved multiple times in Orthotrichum and Ulota, which supports the former hypothesis. Considering morphological statistics, the development of the cryptopore in Orthotrichum may provide increased resilience to dry habitats, and may promote their habitat shift during evolution.