Bacterial-fungal metabolite trade-offs determine their ecological interactions. We designed a non-obligate pairwise metabolite cross-feeding (MCF) between Bacillus amyloliquefaciens and Aspergillus oryzae. Cross-feeding Aspergillus metabolites (MCF-1) affected higher growth and biofilm formation in Bacillus. LC-MS/MS-based multivariate analyses (MVA) showed variations in the endogenous metabolite profiles between the cross-fed and control Bacillus. We observed and validated that Aspergillus-derived oxylipins were rapidly depleted in Bacillus cultures concomitant with lowered secretion of cyclic lipopeptides (CLPs). Conversely, Bacillus extracts cross-fed to Aspergillus (MCF-2) diminished its mycelial growth and conidiation. Fungistatic effects of Bacillus-derived cyclic surfactins were temporally reduced following their hydrolytic linearization. MVA highlighted disparity between the cross-fed (MCF-2) and control Aspergillus cultures with marked variations in the oxylipin levels. We conclude that the pairwise MCF selectively benefitted Bacillus while suppressing Aspergillus, which suggests their ammensalic interaction. Widening this experimental pipeline across tailored communities may help model and simulate BFIs in more complex microbiomes.