Cooksville was once known as "Harrisville" after Daniel Harris, one of its earliest settlers. Cooksville was an important stage coach stop along the Dundas highway (formerly Highway 5), which was carved out of the wilderness after a survey by Asa Danforth in 1798.

The village was renamed in 1836 in honor of its leading entrepreneur, Jacob Cook, who operated the first stagecoach mail service and operated local businesses. Jacob Cook, bought 100 acres (0.40 km²) at Dundas and Hurontario streets for $30 in 1819.

Located at the heart of Toronto Township, Cooksville had been the centre for civic, industrial, commercial, and educational interests for over a century. Mississauga's first municipal offices were located at the corner of Dundas and Hurontario Streets, as was the Central Library, the offices for the public and separate school boards and various Federal and Provincial ministries.

In 1852, a major fire destroyed much of the village, and by 1873, when it was selected over Streetsville as the site of the new Town Hall, it was in need of an economic boost.

A tornado hit the area on June 24, 1923 destroying mostly rural farmhouses around the town. Very little of pre-1940 Cooksville remains. Even the remnants of the old Cooksville Brick and Tile Yard, which provided employment to hundreds of local people from 1912-1970, have recently disappeared beneath new development.

Cooksville was the residence of Grand Duchess Olga Alexandrovna of Russia while in exile in Canada.