Early efforts to classify Mortierellaceae were based on macro- and micromorphology, but sequencing and phylogenetic studies with ribosomal DNA (rDNA) markers have demonstrated conflicting taxonomic groupings and polyphyletic genera. Although some taxonomic confusion in the family has been clarified, rDNA data alone is unable to resolve higher level phylogenetic relationships within Mortierellaceae. In this study, we applied two parallel approaches to resolve the Mortierellaceae phylogeny: low coverage genome (LCG) sequencing and high-throughput, multiplexed targeted amplicon sequencing to generate sequence data for multi-gene phylogenetics. We then combined our datasets to provide a well-supported genome-based phylogeny having broad sampling depth from the amplicon dataset. Resolving the Mortierellaceae phylogeny into monophyletic groups led to the definition of 14 genera, 7 of which are newly proposed. Low-coverage genome sequencing proved to be a relatively cost-effective means of generating a well-resolved phylogeny. The multi-gene phylogenetics approach enabled much greater sampling depth and breadth than the LCG approach, but was unable to resolve higher-level organization of groups. We present this work to resolve some of the taxonomic confusion and provide a genus-level framework to empower future studies on Mortierellaceae diversity, biology, and evolution.