Filamentous fungi native to heavy metals (HMs) contaminated sites have great potential for bioremediation, yet are still often underexploited. This research aimed to assess the HMs resistance and Hg remediation capacity of fungi isolated from the rhizosphere of plants resident on highly Hg-contaminated substrate. Analysis of Hg, Pb, Cu, Zn, and Cd concentrations by X-ray spectrometry generated the ecological risk of the rhizosphere soil. A total of 32 HM-resistant fungal isolates were molecularly identified. Their resistance spectrum for the investigated elements was characterized by tolerance indices (TIs) and minimum inhibitory concentrations (MICs). Clustering analysis of TIs was coupled with isolates’ phylogeny to evaluate HMs resistance patterns. The bioremediation potential of five isolates’ live biomasses, in 100 mg/L Hg2+ aqueous solution over 48 h at 120 r/min, was quantified by atomic absorption spectrometry. New species or genera that were previously unrelated to Hg-contaminated substrates were identified. Ascomycota representatives were common, diverse, and exhibited varied HMs resistance spectra, especially towards the elements with ecological risk, in contrast to Mucoromycota-recovered isolates. HMs resistance patterns were similar within phylogenetically related clades, although isolate specific resistance occurred. Cladosporium sp., Didymella glomerata, Fusarium oxysporum, Phoma costaricensis, and Sarocladium kiliense isolates displayed very high MIC (mg/L) for Hg (140–200), in addition to Pb (1568), Cu (381), Zn (2092–2353), or Cd (337). The Hg biosorption capacity of these highly Hg-resistant species ranged from 33.8 to 54.9 mg/g dry weight, with a removal capacity from 47% to 97%. Thus, the fungi identified herein showed great potential as bioremediators for highly Hg-contaminated aqueous substrates.