Background: Recent reports raise concerns on the changing epidemiology of mpox in the Democratic Republic of the Congo (DRC), with increasing case counts, sexual contact-mediated clusters, and sustained human-to-human transmission driven by a novel monkeypox virus (MPXV) subclade, Clade Ib. Only a limited number of Clade I MPXV genomes have been characterized so far, and they are not representative across different regions and time periods. Methods: We conducted whole genome sequencing of 603 mpox-positive samples that were collected from 581 patients between 2018-2024 in 17/26 provinces of the DRC. Results: For 423 (70.1%) samples the genome coverage was at least 70%, and near full-length MPXV genomes (>90% coverage) were obtained for 348 (57.7%) samples collected from 337 patients. All newly generated MPXV sequences belong to Clade I among which 17 are Clade Ib strains, all from patients infected in 2024 in the South-Kivu province. The remaining new strains fall in previously described Clade Ia groups and potential new groups have also been observed. Genetically diverse MPXV lineages co-circulate in small geographic areas during the same outbreak suggesting multiple zoonotic introductions over a short time period from one or multiple reservoir species. The low number of APOBEC3 mutations in Clade Ia suggests that most human mpox cases are probably linked to zoonotic spillover events. Recent identification of mpox cases in Kinshasa shows that multiple lineages circulate in a large urban center, indicating separate introduction events. Conclusion: The mpox epidemic in the DRC exhibits two distinct patterns. In traditional endemic regions, the epidemic in DRC is predominated by zoonotic spillover events involving Clade Ia. Conversely, in the eastern part of the country, the Clade Ib outbreak is driven by human-to-human transmission highlighting the need for a coordinated response effort at the national, regional and international levels