We mapped X and chromosome 3 quantitative trait loci (QTL) harboring naturally occurring allelic variation for sternopleural and abdominal bristle number. Lines with high (H) and low (L) sternopleural bristle number were derived by artificial selection from a large base population. Isogenic H and L sublines were extracted from the selection lines, and populations of X and third chromosome H/L recombinant isogenic lines were constructed in the homozygous low line background. The polymorphic cytological locations of roo transposable elements provided a dense molecular marker map, with an average inter-marker distance of 4.1 cM. Composite interval mapping was used to infer the map positions and homozygous effects of QTL affecting bristle number. Two X chromosome and six chromosome 3 QTL affecting response to selection for sternopleural bristle number, and three X chromosome and four chromosome 3 QTL affecting correlated response in abdominal bristle number, were detected. Two of the sternopleural bristle and five of the abdominal bristle QTL had sex-specific effects. Significant epistatic interactions were observed between sternopleural bristle number QTL. Many of the intervals containing bristle number QTL coincided with those mapped in previous studies. However, the genomic regions containing bristle number QTL often did not contain obvious candidate loci, and results of quantitative complementation tests to mutations at candidate loci affecting adult bristle number were ambiguous. Further work is necessary to resolve bristle number QTL to the level of genetic loci.