Note: As defined by the US Census Bureau, a city's official boundaries often extend miles beyond the city itself and may even cross county lines. As such, several thousand US cities officially exist in two or more counties (and therefore appear on multiple counties' lists of cities.)
City | Rank | 2024 Pop. | 2020 Pop. | Change | Density (/mi²) | Area (mi²) | Type |
|---|---|---|---|---|---|---|---|
| Brattleboro | 1 | 12,097 | 12,166 | -0.11% | 377 | 32.1 | Town |
| Rockingham | 2 | 4,786 | 4,833 | -0.19% | 116 | 41.4 | Town |
| Westminster | 3 | 3,011 | 3,002 | 0.1% | 67 | 45.0 | Town |
| Bellows Falls | 4 | 2,762 | 2,789 | -0.25% | 2,032 | 1.4 | Village |
| Putney | 5 | 2,605 | 2,614 | -0.19% | 98 | 26.7 | Town |
| Wilmington | 6 | 2,284 | 2,251 | 0.44% | 56 | 40.5 | Town |
| Vernon | 7 | 2,201 | 2,180 | 0.36% | 113 | 19.4 | Town |
| Guilford | 8 | 2,135 | 2,122 | 0.28% | 54 | 39.5 | Town |
| Londonderry | 9 | 1,942 | 1,917 | 0.57% | 55 | 35.5 | Town |
| Dummerston | 10 | 1,889 | 1,863 | 0.37% | 62 | 30.7 | Town |
| Dover | 11 | 1,853 | 1,799 | 0.76% | 52 | 35.8 | Town |
| Marlboro | 12 | 1,782 | 1,725 | 0.91% | 44 | 40.3 | Town |
| Newfane | 13 | 1,656 | 1,643 | 0% | 42 | 39.8 | Town |
| Whitingham | 14 | 1,363 | 1,339 | 0.52% | 37 | 36.8 | Town |
| Townshend | 15 | 1,299 | 1,289 | 0.31% | 31 | 42.3 | Town |
| Jamaica | 16 | 1,005 | 0 | 0.4% | 21 | 48.9 | Town |
| Saxtons River | 17 | 470 | 476 | -0.42% | 1,002 | 0.5 | Village |
| Westminster | 18 | 288 | 286 | 0% | 211 | 1.4 | Village |
| Jacksonville | 19 | 219 | 215 | 0.46% | 192 | 1.1 | Village |
| Newfane | 20 | 92 | 92 | 0% | 523 | 0.2 | Village |
Note: City markers shown outside the county boundary mean that a part of the city extends into this county, but is primarily located in an adjacent county.
Brattleboro is the largest city in Windham County.
Newfane is the smallest city in Windham County.
There are 20 cities in Windham County, Vermont.