Widespread use of di (2-ethylhexyl) phthalate (DEHP) as a plasticizer has caused considerable soil pollution; however, little is known about indigenous microbial communities involved in its degradation in soil. In this study, metagenomic sequencing combined with metabolite determination was used to explore microorganisms and genes potentially involved in DEHP degradation in aerobic and anaerobic soils. The results showed that under both dryland aerobic and flooded anaerobic conditions, DEHP was initially hydrolyzed into mono (2-ethylhexyl) phthalate which was then hydrolyzed into phthalic acid; benzoic acid was the central intermediate during further metabolism steps. Bacteria were more responsive to DEHP presence than fungi/archaea, and potential degradative genes stimulated by DEHP were predominantly associated with bacteria, reflecting the dominant role of bacteria in DEHP degradation. Members of the Actinomycetales seemed to be the dominant degraders under aerobic conditions, while a number of phyla i.e. Gemmatimonadetes, Proteobacteria, Acidobacteria and Bacteroidetes appeared to be involved under anaerobic conditions. Interestingly, ~50% of esterase/lipase/cytochrome P450 genes enriched by DEHP under aerobic conditions were from Nocardioides, a bacterial genus that has not been previously directly linked to phthalate ester degradation. The results indicate that novel degraders may play an important role in DEHP degradation in natural soil environments. This study provides a better understanding of the phthalate ester biodegradation processes occurring in soil.