There are about 200 museums in West Virginia. Most are dedicated to one subject, usually some aspect of history, but there are many that take more than one or two subjects as their mission. Some museums display traveling exhibits on various subjects. Some have diverse permanent collections.

Many are operated by the state or national government in West Virginia. The West Virginia State Museum in the Culture Center in Charleston is the state's oldest, founded in 1905, and has the largest collection, 56,000 objects of history, art, technology, and natural science. Harpers Ferry National Historical Park—which interprets John Brown's Raid, the Civil War, arms manufacturing, and Storer College, the state's first Black institutional of higher learning—is the most visited history-related site in the state. Another much-visited place is the Canyon Rim Visitor Center of the New River Gorge National Park and Preserve near Fayetteville, with a small center at Sandstone. Another, the Seneca Rocks Discovery Center is operated by the U.S. Forest service.

The state also operates Grave Creek Mound Archaeological Complex in Moundsville, the state's largest prehistory museum. Other museums, including the South Charleston Interpretive Center, also have prehistoric-related displays,

Over a one-third of the state parks are historical in nature or have history exhibits. Cass Scenic Railroad State Park's collection of geared, steam, mountain-logging locomotives is unique in the nation. Many state parks include small museums, such as Museum in the Park at Chief Logan State Park, the Mansion House Museum at Tu-Endie-Wei, Berkeley Springs State Park, Fairfax Stone, and Watters Smith Memorial.

Many cities and counties operate museums, including Beckley, Beverly, Clarksburg, Huntington, Shepherdstown, Weirton, Scotts Run, and Morgantown, and most counties, including of Barbour, Brooke, Doddridge, Hancock, Jackson, Jefferson, Marion, Pocahontas, Preston, Randolph, Marshall, Summers, Tyler, and Wetzel (note that some counties are currently more active than others).

There are numerous historic house museums, some privately owned. One of the finest is the Oglebay Mansion Museum in Wheeling. It is one of the four largest museums in West Virginia. Other house museums include Blennerhassett Island Historical State Park near Parkersburg, the Adam Stephen House and Belle Boyd House in Martinsburg, North House Museum in Lewisburg, Pearl S. Buck Birthplace in Hillsboro, North House Museum in Lewisburg, Anna Jarvis Birthplace Museum in Taylor County, Adaland Mansion in Philippi, Campbell Flannagan Murrell House in Hinton, and Madie Carroll House in the Guyandotte section of Huntington, to name just a few.

There are also many historic courthouses. The historic federal building where the statehood debates took place in Wheeling is today a museum, West Virginia Independence Hall.

There are three restored mills. The Easton Roller Mill teaches about a more modern method of flour production than the older grindstone-operated mills at Jackson's Mill and Babcock State Park.

There are several forts, military museums, and battlefield parks. Pricketts Fort is a reconstructed stockade with cabins, where the 18th-century frontier is interpreted. Adjacent to the stockade is the restored early 19th-century Job Prickett House. Civil War sites with small museums include Carnifex Ferry Battlefield State Park and Droop Mountain Battlefield State Park. Fort Ashby is the site of a late 1700s barracks, and Fort Edwards displays artifacts discovered from the largest French & Indian War battle in what is now West Virginia.

Of the numerous glass museums, Oglebay Glass Museum has a superlative collection from five 19th-century glass factories in Wheeling. The Fenton Glass Company has a room with a large selection of the many types of glass that the company made throughout the 20th century. Blenko Glass in Milton has a showroom and gives demonstration. A museum dedicated to Fostoria Glass is in Moundsville. The Museum of American Glass in West Virginia was started in Weston in 1993.

There are several transportation museums, most related to railroads. The Baltimore & Ohio Railroad Museum is located in the 1905 Beaux Arts-style station in Wheeling, now West Virginia Northern Community College. The Collis P. Huntington Railroad Historical Society operates the Huntington Railroad Museum. The city of Elkins also maintains a railroad museum. A John Henry Museum is located in the town of Talcott, Summers County, and the Hinton Railroad Museum is just a few miles away. The Princeton Railroad Museum features exhibits and artifacts of the Virginian Railway. Matewan Depot Welcome Center & Museum offers history about railroads, the Hatfield-McCoy Feud, coal mining, and the Mine Wars. Other depot museums are located in Pennsboro, St. Albans, Rowlesburg, Smithton, Thurmond, Tunnelton, and Gassaway; others are in various states of restoration. The Point Pleasant River Museum burned in the early 2020s but has re-opened at a new location in that city.

Also related to the Hatfield-McCoy Feud is the Hatfield Homeplace & Museum at Sarah Ann, Logan County.

Restored schools and education museums include the Irish Corner, a one-room school restored by the Nicholas County Historical Society in Memorial Park in Summersville. Contentment at Ansted interprets the life and industrial career of George Imboden but also includes a restored one-room schoolhouse. The Graham House in Summers County is an 18th-century residence with a restored one-room schoolhouse. Although not a one-room school house, the General Thomas M. Harris School Museum in Harrisville is operated by the Ritchie County Historical Society.

There are several farm-related museums, including the West Virginia State Farm Museum at the Mason County Fairgrounds near Point Pleasant and the Heritage Farm Museum & Village in Wayne County.

Art museums include the Huntington Museum of Art housed in the Bauhaus-style building designed by architect Walter Gropius. There, the museum shows its important permanent collection and a regular program of changing exhibitions. It is one of the four largest museums. Carnegie Hall, which also features a large theater, is in Lewisburg. Oglebay, West Virginia University, and the Clay Center for the Arts & Sciences also feature art galleries.

Children's museums include the Youth Museum of Southern West Virginia in Beckley. In 2000, it received a prestigious national award from the National Endowment for the Arts. The Buckskin Area Council Boy Scout Museum in Charleston is the largest such museum, although there are good scout exhibits in other museums. Sunrise Museum, previously located in Sunrise Mansion in Charleston and one of the four largest museums, changed its name to the Avampato Discovery Center and moved to a new home in the Clay Center for the Arts & Sciences in 2003. Wheeling is home to the Children's Museum of the Ohio Valley, in addition to youth attractions at Oglebay Park and the Kruger Street Toy & Train Museum.

There are numerous science museums and nature centers. The Museum of Radio and Technology in Huntington shows the development of electronic technology in the 20th century. The Core Arboretum at West Virginia University is one of three arboretums. The Good Children's Zoo in Oglebay Park and the West Virginia Wildlife Center in French Creek are the two most prominent zoos in the state. The Forks of Coal State Natural Area near the Kanawha-Lincoln line also has some live animals and interprets that watershed. The Appalachian Forest National Heritage Area features exhibits that celebrate the central Appalachian forest. The National Radio Astronomy Observatory in Green Bank include interactive science exhibits.

West Virginia University has several museums. The Royce J. and Caroline B. Watts Museum in Morgantown, part of West Virginia University, examines the social, cultural, and technological histories of natural resources in the state. The Cook-Hayman Pharmacy Museum at West Virginia University is the only pharmacy museum. The William A. Neal Museum of the Health Sciences is an interdisciplinary institution.

There are several coal institutions. The Exhibition Coal Mine and Coal Camp in Beckley exhibits methods of mining and mining artifacts. The West Virginia Mine Wars Museum, established in 2015 in Matewan, interprets events of the state's turbulent coal-labor relationship in the early 1900s. Madison is home to the Coal Heritage Museum, and the National Coal Heritage Area has a visitor center in Bramwell.

African American museums include he African Zion Baptist Church and the Freedom Cabin, showing what life was like when Booker T. Washington was a child in Malden.

Religious sites include the Rehoboth Church Museum in Union, Monroe County, one of three 18th-century log buildings in the state. Perhaps the state's most famous site in this category is the International Mother's Day Shrine in Grafton. In addition, the West Virginia Baptist Historical Society maintains artifacts and archives at its home in Jackson County.

At least two sites are related to the Great Depression and New Deal. Arthurdale is home to a New Deal Homestead Museum, and the state CCC Museum is at Quiet Dell, Harrison County.

Some of the newer museums tie into the cryptid craze, including the Mothman Museum in Point Pleasant and Flatwoods Monster Museum the state Bigfoot Museum in Sutton.

The West Virginia Association of Museums was organized in 1990 to strengthen the state's museums individually and as a group. Every year an annual conference is held, and workshops are presented on a variety of specialized subjects including conservation of objects, basic museum operations, cataloging, disaster preparedness, and interpretation.