FANCJ mutations are linked to the chromosomal instability disorder Fanconi anemia (FA) and increase breast cancer risk. FANCJ encodes a DNA helicase implicated in homologous recombination (HR) repair of double‐strand breaks (DSBs) and interstrand cross‐links (ICLs), but its mechanism of action is not well understood. Live cell imaging demonstrates that FANCJ recruitment to laser‐induced DSBs, but not psoralen‐ICLs, is dependent on nuclease‐active MRE11 and independent of BRCA1. Inhibition of MRE11 nuclease by Mirin adversely affected FANCJ localization to laser‐induced DSBs, but not psoralen‐ICLs. FANCJ is required for timely recruitment of Bloom's syndrome helicase and CtIP to DSBs in vivo. FANCJ directly interacts with MRE11 and inhibits its exonuclease activity in a specific manner, suggesting that FANCJ harnesses MRE11 nuclease to facilitate DSB processing and appropriate end resection. Spontaneous or IR‐induced chromosomal instability in FANCJ‐depleted cells is suppressed when MRE11 is depleted. Interplay between FANCJ and MRE11 insures a normal response to IR‐induced DSBs, whereas FANCJ involvement in ICL repair is regulated by MLH1 and FANCA, but not FANCD2. Thus, MRE11 helps to recruit FANCJ to DSBs and FANCJ can modulate MRE11 nuclease activity at DNA ends, consistent with a collaborative role of FANCJ and BLM helicases with MRE11 in strand resection.