Ironically, the original specimen was of the black-plumaged subspecies from Dirk Hartog Island, which was not recorded again for 80 years. Meanwhile, the widespread blue-plumaged subspecies was discovered and described as two separate species by John Gould in 1865. He called one specimen collected from inland New South Wales the White-winged Superb Warbler, M. cyanotus, while another, which appeared to have a white back and wings, was described as M. leuconotus, the White-backed Superb Warbler. It was not until the early 20th century that both of these blue-plumaged mainland forms were found to be of a single species. George Mack, ornithologist of the National Museum of Victoria, considered the specific name leuconotus to take precedence in his 1934 revision of the genus, and more recent studies have followed suit. The back region between the shoulders is in fact bare, with feathers that arise from the shoulder (scapular) region and sweep inwards in different patterns. This variation confused the early naturalists who described the white-backed and blue-backed species.
The White-winged Fairy-wren was often referred to as the Blue-and-white Wren, and early observers, such as Norman Favaloro of Victoria, refer to them by this name. However, like other fairy-wrens, the White-winged Fairy-wren is unrelated to the true wren (family Troglodytidae). It was previously classified as a member of the old world flycatcher family Muscicapidae, and later as a member of the warbler family Sylviidae, before they were placed in the newly recognised Maluridae in 1975. More recently, DNA analysis has shown the Maluridae family to be related to the Meliphagidae (honeyeaters), and the Pardalotidae (pardalotes, scrubwrens, thornbills, gerygones and allies) in the large superfamily Meliphagoidea.
Within the Maluridae, it is one of 12 species in the genus, Malurus. It is most closely related to the Australian Red-backed Fairy-wren, with which it makes up a phylogenetic clade with the White-shouldered Fairy-wren of New Guinea as the next closest relative. Termed the bicoloured wrens by ornithologist Richard Schodde, these three species are notable for their lack of head patterns and ear tufts and their uniform black or blue plumage with contrasting shoulder or wing colour; they replace each other geographically across northern Australia and New Guinea.
M. l. leucopterus and M. l. edouardi are both generally smaller than their mainland relatives, and both subspecies tend to have smaller family groups that consist of only one male and one female, with an occasional helper bird. While the island species and mainland species have been found to have similar social structure, breeding pairs on both islands have, on average, smaller clutches, longer incubation times, and fewer live fledglings. Additionally, while M. l. leuconotus is considered of Least Concern by the IUCN due to its widespread occurrence, both island subspecies are considered vulnerable by the Australian government due to their delicate nesting sites that are easily disturbed by human construction and habitation.
There are three theories as to how the three races of White-winged Fairy-wren could have evolved. The first suggests that black-and-white plumage is an ancestral condition and, following separation of the three populations, blue-and-white plumage evolved in the mainland species. The second hypothesis suggests that black-and-white plumage evolved convergently on the two separate islands. The third suggests that black-and-white plumage evolved once from the blue-and-white ancestral condition, and later the mainland species re-evolved blue plumage.
The distribution of the three bi-coloured fairy-wren species indicates their ancestors lived across New Guinea and northern Australia in a period when sea levels were lower and the two regions were joined by a land bridge. Populations became separated as sea levels rose, and New Guinea birds evolved into the White-shouldered Fairy-wren, and Australian forms into the Red-backed Fairy-wren and the arid-adapted White-winged Fairy-wren.
Measuring 11–13.5 cm (4⅓–5⅓ in) in length, White-winged Fairy-wrens are one of the two smallest species of Malurus. Males typically weigh between 7.2 g (0.25 oz) and 10.9 g (0.38 oz) while females weigh between 6.8 g (0.24 oz) and 11 g (0.39 oz). Averaging in males and in females, the bill is relatively long, narrow and pointed and wider at the base. Wider than it is deep, the bill is similar in shape to those of other birds that feed by probing for or picking insects off their environs. It is finer and more pointed in this species than in other fairy-wrens.
Fully mature adults are sexually dimorphic, with the male being larger and differing in colour from the female. The adult female is sandy-brown with a very light blue tail, and a pinkish buff bill. The male in breeding plumage has a black bill, white wings and shoulders, and a wholly cobalt blue or black body (depending on subspecies). These contrasting white feathers are especially highlighted in flight and ground displays in breeding season. The male in eclipse plumage resembles the female, though it may be distinguished by its darker bill. Both sexes have long, slender, distinct tails held at an upward angle from their bodies. Measuring around 6.25 cm (2½ in), the tail feathers have a white fringe, which disappears with wear.
Nestlings, fledglings, and juveniles have brown plumage and pink-brown bills with shorter tails than adults. Young males develop blue tail feathers and darker bills by late summer or autumn (following a spring or summer breeding season), while young females develop light blue tails. By the subsequent spring, all males are fertile and have developed cloacal protuberances, which store sperm. In contrast, during the breeding season, fertile females develop oedematous brood patches, which are bare areas on their bellies. Males entering their second or third year may develop spotty blue and white plumage during the breeding season. By their fourth year, males have assumed their nuptial plumage, where the scapulars, secondary wing coverts, and secondary flight feathers are white while the rest of their bodies are a vibrant cobalt blue. All sexually mature males moult twice a year, once before the breeding season in winter or spring, and again afterwards in autumn; rarely, a male may moult directly from nuptial to nuptial plumage. The breeding males' blue plumage, particularly the ear-coverts, is highly iridescent due to the flattened and twisted surface of the barbules. The blue plumage also reflects ultraviolet light strongly, and so may be even more prominent to other fairy-wrens, whose colour vision extends into this part of the spectrum.
White-winged Fairy-wrens live in complex social groups. Clans consist of 2–4 birds, typically one brown or partially blue male and a breeding female. Nest helpers are birds raised in previous years which remain with the family group after fledging and assist in raising young; they may be male that have retained their brown plumage, or female. Birds in a group roost side-by-side in dense cover and engage in mutual preening. Several subgroups live within one territory and make up a clan, which is presided over by one blue (or black) male who assumes breeding plumage. While the blue male is dominant to the rest of the brown and partially blue males within his clan, he nests with only one female and contributes to the raising of only her young. It is unclear whether or not he fathers young in any of the other nests within his territory.
Each clan has a specified area of land that all members contribute to foraging from and defending. Frequently, territory sizes, normally 4–6 ha (10–15 acres), are correlated with the abundance of rain and resources in a region; smaller territories occur where insects and resources are plentiful. Additionally, the feeding territories are larger during the winter months when these birds spend much of their time foraging with the entire clan. White-winged Fairy-wrens occupy much larger territories than other fairy-wren species. Observed in this species, the wing-fluttering display is seen in several situations: females responding, and presumably acquiescing, to male courtship displays, juveniles begging for food, by helpers to older birds, and immature males to senior ones. The fairy-wren lowers its head and tail, outstretches and quivers its wings and holds its beak open silently.
Both the male and female adult White-winged Fairy-wren may utilise a rodent-run display to distract predators from nests with young birds. The head, neck and tail are lowered, the wings are held out and the feathers are fluffed as the bird runs rapidly and voices a continuous alarm call.
During another courtship display the male bows deeply forward facing the female, reaching the ground with his bill and spreading and flattening his plumage in a near-horizontal plane for up to 20 seconds. In this pose, the white plumage forms a striking white band across his darker plumage.
Breeding females begin to build their nests in the spring and construct domed structures composed of spiderwebs, fine grasses, thistle-down, and vegetable-down, typically 6–14 cm (2⅓–5½ in) tall and 3–9 mm thick. Each nest has a small entrance on one side and they are normally placed in thick shrubs close to the ground. A clutch of 3–4 eggs is generally laid anywhere from September to January, with incubation lasting around 14 days. The White-winged Fairy-wren generally breeds in the spring in the southwest of Western Australia, but is more opportunistic in arid regions of central and northern Australia, with breeding recorded almost any month after a period of rainfall. Incubation is by the breeding female alone, while the breeding male (a brown or blue male) and nest helpers aid in feeding the nestlings and removing their fecal sacs. The newly hatched nestlings are altricial, gaping immediately for food, and developing downy feather tracts and opening their eyes by the third or fourth day. Nestlings remain in the nest for 10–11 days, and fledglings continue to be fed for 3–4 weeks following their departure from the nest. Fledglings then either stay on to help raise the next brood or move to a nearby territory. It is not unusual for a pair bond to hatch and raise two broods in one breeding season, and helpers tend to lessen the stress on the breeding female rather than increase the overall number of feedings. Like other fairy-wrens, the White-winged Fairy-wren is particularly prone to parasitic nesting by the Horsfield's Bronze-Cuckoo (Chalcites basalis). Parasitism by the Shining Bronze-Cuckoo (C. lucidus) and Black-eared Cuckoo (C. osculans) is rarely recorded.