It was known as Tsoliikawai (ćol:ik:o=wi),[5] meaning "blackbird field", a name also applied to the village, tribe or tribelet at the site.

In 1855, a post office was established in Windsor and Hiram Lewis, a Pony Express rider, became the town's first postmaster.

The Northwestern Pacific Railroad was completed through the town in 1872, providing a faster and cheaper link to the Bay Area.

[7] The Great San Francisco Earthquake caused major damage to numerous buildings in Windsor, many of which were still in the process of repair and reconstruction from 1905 fire.

[7] During World War II, a United States Army Air Forces training air base (currently the Charles M. Schulz – Sonoma County Airport) was built in southern Windsor, and it was common to hear fighter aircraft and bombers flying over the town.

Prior to that, Windsor's economy was predominately based on agricultural work, mainly involving wine grapes.

[12] In January 1998, Windsor voters approved a twenty-year urban growth boundary (UGA), with 72% in favor.

[15] According to the United States Census Bureau, the Town has a total area of 7.3 square miles (19 km2), of which only 0.34% is water.

Children and families benefit from continued support of toy drives, Easter egg hunts, and holiday activities.

Windsor is home to several other community events in coordination with local non-profits and standing citizen advisory groups.

Events include the annual Earth Day and Wellness Festival, Windsor Days Parade, Cinco de Mayo Festival, and the Community Art and Flower Show, live entertainment, recreation class demonstrations, event information booths, and food vendors and spring produce sales from the Windsor Farmer's Market.

Every November, friends and family join with the public to honor home-grown, active-duty service men and women during a Military Banner Red Carpet Ceremony.

Businesses, individuals, students and groups showcase their talents in design and decorating with their themed trees which draw thousands of visitors to the Grove during the month of December.

It is a highlight of the annual Town of Windsor's Holiday Celebration on the Green evening event on the first Thursday in December.

It is located in the historic Hembree House adjacent to the Town's recreational senior center facility.

Most park amenities include a variety of sports fields, play structures, restrooms and picnic areas.

Local regional parks offer hundreds of acres with varied terrain and scenic views.

[27] On April 8, 2021, the San Francisco Chronicle published an article where four women accused then Mayor Dominic Foppoli of sexual assault between 2003 and 2019.

Following that, five more women came forward accusing Foppoli of sexual assault, leading to public outrage and calls for him to resign.

[28] Foppoli officially resigned on May 21, 2021, after reality TV personality Farrah Abraham publicly accused him of sexually assaulting her.

This led to national attention put onto the town and the extreme pressure finally pushed Foppoli to leave office.

The Town of Windsor is a very bicycle friendly community and won an award in 2015 from The League of American Bicyclists.

The initial operating segment between San Rafael and Charles M. Schulz–Sonoma County Airport opened in 2017, three miles short of Windsor.

By April 2016, SMART made known it was seeking up to $38 million in state cap-and-trade funds to extend passenger service north.

[38] In 1992, the Town of Windsor voted to contract with the Sonoma County Sheriff's Office for the provision of law enforcement services.