Aurachins are a small family of natural products with a quinoline chromophore substituted by a farnesyl chain at position 3 or 4, which act as potent inhibitors of respiratory chain electron transport and exhibit antimicrobial, antifungal, and antiplasmodial activities. They were first isolated from myxobacterium Stigmatella aurantiaca Sg a15, and later from the same strain and an actinobacterial strain Rhodococcus sp. During a search for bioactive secondary metabolites from microorganisms in special niches, a new aurachin-type compound, aurachin SS (1), together with two known compounds, aurachin C (2) and aurachin D (3), was isolated from Streptomyces sp. NA04227. This strain was isolated from an earwig (Forficula auricularia) collected in Qixia Mountain, Nanjing, China. Isolation was achieved through large-scale fermentation and a combination of chromatographic methods including normal phase, C-18 silica gel, and Sephadex LH-20. Compound 1 was obtained as a brown oil, with a molecular formula of C21H27NO2 determined by HRESIMS. Its structure, elucidated using 1H, 13C, HSQC, HMBC, and COSY NMR, features a unique geranyl side chain, a methyl-substituted quinoline moiety, a methoxyl group, and an N-oxide group. The whole genome of Streptomyces sp. NA04227 was sequenced and analyzed using antiSMASH, revealing a biosynthetic gene cluster (sau) for aurachins. Based on the genetic organization and sequence identities, a biosynthetic pathway was proposed: anthranilic acid is activated by SauE, extended by minimal PKS, prenylated by SauA (which can accept geranyl pyrophosphate to form the geranyl side chain of 1), hydroxylated by P450 enzymes (SauPI or SauPII), and methylated by an unidentified methyltransferase. Antimicrobial activity assays showed that compounds 2 and 3 had potent activity against Staphylococcus aureus, Streptococcus pyogenes, Bacillus subtilis, and Micrococcus luteus with MICs ranging from 4.0 to 16.0 μM, while aurachin SS (1), with a shorter side chain, exhibited moderate activity with MICs from 32.0 to 64.0 μM. In summary, one new and two known aurachins were isolated and identified from an earwig-associated Streptomyces sp. NA04227. The new compound, aurachin SS (1), is distinct from typical aurachin-type compounds due to its unique geranyl side chain. A unified biosynthetic pathway was proposed based on the identified gene cluster, and the compounds showed moderate to potent antibacterial activity against four tested bacteria.