Heavy metal induced co-selection of antibiotic resistance genes (ARGs) has become an emerging environmental issue. The guts of soil fauna offer a unique habitat in the terrestrial ecosystem and harbor a variety of microorganisms. However, the effects of heavy metals on the gut-associated ARGs of soil fauna are poorly understood. In the present study, collembolans were cultivated with four types of heavy metals (Zn, Cu, Cd, and Cr) and one antibiotic (oxytetracycline), to investigate their impact on the gut-associated ARGs. High-throughput quantitative PCR and 16S rRNA gene amplicon sequencing were used to examine changes in the gut-associated ARGs and microbial composition caused by the metals and antibiotic. The results showed that heavy metals alone induced co-selection of ARGs in the collembolan gut, but the effects were weaker than selection by oxytetracycline. When Zn or Cu was present together with oxytetracycline, there was a strong synergistic effect between the compounds, which increased the selection of ARGs in the collembolan guts. Furthermore, redundancy analysis revealed that the gut microbiota and mobile genetic elements (MGEs) were significantly correlated with the ARG composition. These results extend our understanding on effects of heavy metals on the dispersal of ARGs in the soil food web.