Heavy metal pollution has important effects on ecosystem nitrogen (N) cycling, but factors driving differences between the direction, onset and intensity of responses are poorly understood. We used two contrasting grassland soils to examine the effects of copper (Cu) on the abundance and activity of N cycling microbial guilds and plant responses, including plant δ¹⁵N as an integrator of the N cycle. A low pH sandy soil and a high pH sandy loam soil were aged two years in outdoor mesocosms with copper (Cu) treatments of background, 200, 400 or 1000 mg kg⁻¹ Cu. After two years, increased Cu treatments resulted in significantly lower abundances of ammonia oxidizing archaea, Nitrospira nitrite oxidizing bacteria (NOB), potential ammonia oxidation rates and plant biomass in both soils. Plants possessed significantly increased N content and enriched shoot δ¹⁵N in with higher Cu in both soils. While abundances of ammonia oxidizing bacteria were unaffected by Cu, the response among Nitrobacter NOB and denitrifiers and plant δ¹³C differed between the two soils. In contrast to plants, differences in the intensity and direction of microbial guild responses were not explained by increasing soluble Cu but rather shaped by soil type. This indicates that the two soils differed in metal bioavailability to plants, as well as harbored microbial communities with inherent differences in metal sensitivity. Furthermore, effects of increasing Cu on microbial N-cycling guilds became more apparent with longer incubation time, emphasizing the importance of long-term studies to assess important ecosystem effects of Cu contamination. Taken together, we conclude that a combination of plant and microbial responses can give better insights on how Cu is affecting the N cycle in polluted soils.