The body structure of Dimorphodon displays many "primitive" characters, such as, according to Owen, a very small brain-pan and proportionally short wings. The first phalanx in its flight finger is only slightly longer than its lower arm. The neck was short but strong and flexible and may have had a membraneous pouch on the underside. The vertebrae had pneumatic foramina, openings through which the air sacks could reach the hollow interior. Dimorphodon had an adult body length of 1 metre (3.3 ft) long, with a 1.45 metre (4.6 ft) wingspan. The tail of Dimorphodon was long and consisted of thirty vertebrae. The first five or six were short and flexible but the remainder gradually increased in length and were stiffened by elongated vertebral processes. The terminal end of the tail may have borne a Rhamphorhynchus-like tail vane, although no soft tissues have yet been found of Dimorphodon to confirm this speculation.
Dimorphodon had a large, bulky skull approximately 22 centimetres in length, whose weight was reduced by large openings separated from each other by thin bony partitions. Its structure, reminiscent of the supporting arches of a bridge, prompted Richard Owen to declare that, in far as achieving great strength from light-weight materials was concerned, no vertebra was more economically constructed; Owen saw the vertebrate skull as a combination of four vertebrae modified from the ideal type of the vertebra. The front of the upper jaw had four or five fang-like teeth followed by an indeterminate number of smaller teeth; the maxilla of all exemplars is damaged at the back. The lower jaw had five longer teeth and thirty to forty tiny, flattened pointed teeth, shaped like a lancet. Many depictions give it a speculative puffin-like 'beak' because of similarities between the two animals' skulls.
The first fossil remains now attributed to Dimorphodon were found in England by fossil collector Mary Anning, at Lyme Regis in Dorset, UK in December 1828. This region of Britain is now a World Heritage Site, dubbed the Jurassic Coast; in it layers of the Blue Lias are exposed, dating from the Hettangian-Sinemurian. The specimen was acquired by William Buckland and reported in a meeting of the Geological Society on 5 February 1829. In 1835, after a thorough study by William Clift and William John Broderip, this report, strongly expanded, was published in the Transactions of the Geological Society, describing and naming the fossil as a new species. As was the case with most early pterosaur finds, Buckland classified the remains in the genus Pterodactylus, coining the new species Pterodactylus macronyx. The specific name is derived from Greek makros, "large" and onyx, "claw", in reference to the large claws of the hand. The specimen, presently NHMUK PV R 1034, consisted of a partial and disarticulated skeleton on a slab, lacking the skull. Buckland in 1835 also assigned a piece of jaw from the collection of Elizabeth Philpot to P.macronyx. Later, the many putative species assigned to Pterodactylus had become so anatomically diverse that they began to be broken into separate genera.
In 1858, Richard Owen reported the find of two new specimens, NHMUK PV R 41212 and NHMUK PV R 1035, again partial skeletons but this time including the skulls. Having found the skull to be very different from that of Pterodactylus, Owen assigned Pterodactylus macronyx its own genus, which he named Dimorphodon. His first report contained no description and the name remained a nomen nudum. In 1859 however, a subsequent publication by Owen provided a description. After several studies highlighting aspects of Dimorphodon's anatomy, Owen in 1874 made NHMUK PV R 1034 the holotype.
Meanwhile, though Dimorphodon is not a very common fossil, other fragmentary specimens were found. Some of these were acquired by Othniel Charles Marsh between 1873 and 1881 from the London fossil dealer Bryce McMurdo Wright. One of these had been recovered from early Jurassic strata at the south bank of the Severn river, at the Aust Cliff.
On another hand, an additional species of Dimorphodon, D. weintraubi was named by James Clark et al in 1998 from a partial skeleton recovered in siltstones from the site Huizachal Canyon in La Boca Formation in Tamaulipas, Mexico, from the Early Jurassic (Pliensbachian), where remains of sphenodontians, dinosaurs and mammaliaforms have also been found . It is known from the type specimen, IGM 3494 (Instituto Geológico de México, of the Universidad Nacional Autónoma de México), that comprises articulated pieces of the skeleton including the posterior part of skull, four cervical vertebrae, the scapulocoracoids, left humerus, partial right wing and right leg distal to mid tibiotarsus. This specimen is larger than D. macronyx and the well preserved foot of it shows that pterosaurs do not have a digitigrade posture in their hindlimbs, but that it have a plantigrade gait, as has been inferred from footprints. The name of the species is a homage to Dr. Robert L. Weintraub.