Insects, despite their diversity on Earth now, were latecomers compared to other arthropods. The oldest insect fossil may be a head of Rhyniognatha hirsti from the early Devonian (about 410 million years ago). A priest found it in 1919 in Scotland, but its importance was realized only recently. In 2004, paleontologists discovered that the way the mandibles of the mouthparts attached to the head meant that it was a true insect. The earliest definite fossil insects are from the about 390 million years ago, found in North America. They were bristletails, a group that survives today, representing the most primitive lineage of insects. A huge diversification of insects followed during the late Carboniferous (330 to 300 million years ago). At least twelve major lineages specialized into different feeding modes, such as varied types of plant-eaters (herbivores) and those that fed on dead organisms (detritivores). By 100 million years ago, the major groups of insects looked much like what we see now.

Arthropods have been on Earth for more than 540 million years, and were diverse almost from the beginning. Different lineages of arthropods, such as crustaceans, diverged as early as 525 million years ago. The evolution of an external body covering (the exoskeleton), and the presence of body segments and paired appendages (mouthparts, legs, claws, antennae) signaled the transition from early worm-like precursors to arthropods. While modern arthropods live in nearly every habitat, the earliest arthropods were probably tiny, bottom-dwellers scavenging detritus at the bottom of warm seas. The enormous success of arthropods is at least partly due to their appendages. Located on all body regions, their appendages became specialized especially for feeding through the mouthparts, but also for getting oxygen through respiration (gills), reproducing (elaborate external genitalia), and moving around including walking, swimming, and/or flying. The gradual adoption of a modular body plan with multifunctional appendages has allowed arthropods to thrive in an impressive variety of environments.