African swine fever (ASF) is the most lethal disease of pigs caused by ASF virus (ASFV) with severe economic implications and threat to food security in endemic countries. Between 2016 and 2018, several ASF outbreaks were reported throughout pig producing States in Nigeria. This study was designed to identify the ASFV genotypes responsible for these outbreaks and the transmission pathways of the virus during this period. Twenty-two ASFV-positive samples collected during passive surveillance in eight States of Nigeria were characterized using 3 partial genes sequences of the virus. The genes were: p72 capsid protein of the B646L, p54 envelope protein of E183L, and the central variable region (CVR) within B602L of ASFV. Phylogenetic analysis based on p72 and p54 revealed ASFV genotype I as the circulating virus. Sequence analysis of the CVR of B602L revealed genetic variations with six ASFV variants namely: Tet-15, Tet-20a, Tet-21b, Tet-27, Tet-31 and Tet-34, thus increasing the overall genetic diversity of ASFV in Nigeria. Three of these variants: Tet-21b, Tet-31 and Tet-34 were identified for the first time in Nigeria. The new variants of ASFV genotype I were identified in the States of Enugu, Imo, Plateau and Taraba, while co-circulation of multiple variants of ASFV genotype I were recorded in Plateau and Benue States. The high genetic diversity, emergence and increasing recovery of new variants of genotype I in Nigeria should be a concern given that ASFV is a relatively stable DNA virus. The epidemiological implications of these findings require further investigation.