We investigated fast and slow muscle fiber transcriptome exercise dynamics among three groups of men: Lifelong exercisers (LLE, n=8, 74±1 y), old healthy non-exercisers (OH, n=9, 75±1 y), and young exercisers (YE, n=8, 25±1 y). Muscle biopsies were obtained pre- and 4h post-resistance exercise (3x10 knee extensions, 70% 1-RM). Fast and slow fiber size and function were assessed pre-exercise with fast and slow RNA-seq examined pre- and post-exercise. LLE fast fiber size was similar to OH, which were ~30% smaller than YE (P<0.05) with contractile function variables among groups resulting in lower power in LLE (P<0.05). LLE slow fibers were ~30% larger and more powerful compared to YE and OH (P<0.05). At the transcriptome level, fast fibers were more responsive to resistance exercise compared to slow fibers among all three cohorts (P<0.05). Exercise induced a comprehensive biological response in fast fibers (P<0.05) including transcription, signaling, skeletal muscle cell differentiation, and metabolism with vast differences among the groups. Fast fibers from YE exhibited a growth and metabolic signature, with LLE being primarily metabolic, and OH showing a strong stress related response. In slow fibers, only LLE exhibited a biological response to exercise (P<0.05), which was related to ketone and lipid metabolism. The divergent exercise transcriptome signatures provide novel insight into the molecular regulation in fast and slow fibers with age and exercise and suggest that the ~5% weekly exercise time commitment of the lifelong exercisers provided a powerful investment for fast and slow muscle fiber metabolic health at the molecular level.