Crepidotus subg. Dochmiopus contributes to more than half of Crepidotus species and exhibits highly hidden diversity. However, C. subg. Dochmiopus is challenging to study because the basidiomata of C. subg. Dochmiopus species are usually small and white, inconspicuous interspecific distinctions, and possess a familiar complex. In this study, we utilized a variety of characteristics for species identification, including habitat, presence or absence of a stipe in mature specimens, pileipellis and cheilocystidia patterns, whether the lamellae edges are fimbriated, and other characteristics. Above all, cheilocystidia and pileipellis patterns will be important in C. subg. Dochmiopus research. Based on the present specimens, we constructed a multigene phylogenetic tree (ITS + LSU) and recognized four new species: C. lamellomaculatus sp. nov., C. capitatocystidiatus sp. nov., C. succineus sp. nov., C. clavocystidiatustustus sp. nov. Detailed morphological descriptions, photographs, line drawings and comparisons with closely related taxa for the new species are provided. The current phylogenetic analysis does not support the previously classifications, indicating that the classification of Crepidotus requires re-evaluation. But the existing molecular datasets and species’ descriptions are insufficient to fully resolve the classification. Further integration of new gene segments and a comprehensive review of morphological characteristics will reveal a natural classification for Crepidotus.