It is a variable species, much like the related fox sparrow (Passerella iliaca), and its systematics are still not completely resolved.

The dark-eyed junco was formally described by the Swedish naturalist Carl Linnaeus in his landmark 1758 10th edition of Systema Naturae as Fringilla hyemalis.

[2] Linnaeus based his description on the "Snow-Bird" that Mark Catesby had described and illustrated in his 1731 The Natural History of Carolina, Florida and the Bahama Islands.

[italics in original][3]The type locality was restricted to South Carolina by the American Ornithologists' Union in 1931.

[10] They breed in the North American boreal forests from Alaska to Newfoundland and south to the Appalachian Mountains, wintering throughout most of the United States.

These eight subspecies have blackish-gray heads and breasts with brown backs and wings and reddish flanks, tending toward duller and paler plumage in the inland and southern parts of its range.

[12][10] Sometimes included with the gray-headed dark-eyed junco proper as part of the gray-headed group, this subspecies differs from it in having a more silvery bill[11] with a dark-colored upper mandible and a light-colored lower mandible,[12][10] a variable amount of rust on the wings, and pale underparts.

The extremely rare Guadalupe junco (Junco insularis) was formerly considered to be a subspecies of this species (either included in the gray-headed group or placed in a seventh group of its own, the Guadalupe group), but is now treated as a separate species in its own right – perhaps a rather young one, but certainly this population has evolved more rapidly than the 14 or 15 subspecies of the dark-eyed junco on the mainland due to its small population size and the founder effect.

[14] Juveniles often have pale streaks on their underparts and may even be mistaken for vesper sparrows (Pooecetes gramineus) until they acquire adult plumage at two to three months, but dark-eyed junco fledglings' heads are generally quite uniform in color already, and initially their bills still have conspicuous yellowish edges to the gape, remains of the fleshy wattles that guide the parents when they feed the nestlings.

The dark-eyed junco's breeding habitat is coniferous or mixed forest areas throughout North America.

[16] Northern birds migrate further south, arriving in their winter quarters between mid-September and November and leaving to breed from mid-March onwards, with almost all of them gone by the end of April or so.

[16][17] Many populations are permanent residents or altitudinal migrants, while in cold years they may choose to stay in their winter range and breed there.

Seasonally sympatric females show difference in migration and reproductive timing that is dependent on hormone and ovary regulation.

[18] The migrant female J. hyemails experience delayed growth in the gonad to allow time for their seasonal migration.

They then migrate down to the northeastern United States, where the resident subspecies is the Carolina dark-eyed junco (J. h. carolinensis).

Female Carolina dark-eyed juncos have large ovaries and, therefore, do not experience gonadal growth delays because they are residents in the area.

In winter, dark-eyed juncos are familiar in and around towns, and in many places are the most common birds at feeders.

[12] The slate-colored dark-eyed junco (J. h. hyemalis) is a rare vagrant to Western Europe and may successfully winter in Great Britain, usually in domestic gardens.

[19] However, during the breeding season, insects comprise nearly half of the diet of adult dark-eyed juncos.

The slightly glossy eggs are grayish or pale bluish-white and heavily spotted (sometimes splotched) with various shades of brown, purple or gray.

This is due to exceptionally high phenotypic diversity, as seen in the large number of color patterns, over what seems to be a very short amount of time.

Postglacial theory is supported by yellow-eyed and dark-eyed juncos sharing a dominant haplotype in their mitochondrial DNA, which indicates a recent burst in population.

The range of red-backed (J. h. dorsalis) and grey-headed juncos (J. h. caniceps) in the south of North America also provides evidence, as the two seem to represent successive steps in developing dark-eyed forms.

Isolation barriers created by unsuitable desert habitat likely led to this lack of gene flow.

Much of this is modeled through a population of dark-eyed juncos living on the University of California, San Diego's campus.

However, genome analysis reveals that the population was likely established from the coastal subspecies J. h. pinosis 20–30 generations ago, which are conditions that make the founder effect very likely to be relevant.

Selection is likely magnifying changes initially driven by drift, allowing the UCSD population to diverge from its neighbors very quickly.

Two of the most differentiated genes between the ancestral J. h. pinosis population and the UCSD birds were linked to beneficial traits for urban environments.

Variation in KCNQ4 is linked to high-frequency echolocation in bats, and seems to correlate with making higher pitched calls.

Research remains to be done on which alleles in the UCSD population serve an adaptive function, and which are likely just consequences of drift.