Blakeman ruled Stratford until his death in 1665, but as the second generation of Stratford grew up many of the children rejected what they perceived as the exceptional austerity of the town's founders. This and later generations sought to change the religious dictums of their elders, and the utopian nature of Stratford and similar communities was gradually replaced with more standard colonial administration. By the late 1600s, the Connecticut government had assumed political control over Stratford.

Many descendants of the original founding Puritan families remain in Stratford today after over 350 years; for centuries they often intermarried within the original small group of 17th century Pilgrim families. Stratford's original name was Cupheag, but was later changed to honor Stratford upon Avon in England. Despite its Puritan origins, Stratford was the site of the first Anglican church in Connecticut, founded in 1707 and ministered by the Rev. Dr. Samuel Johnson. Settlers from Stratford went on to found other American cities and towns, including Newark, New Jersey, established in 1666 by members of the Stratford founding families who believed the town's religious purity had been compromised by the changes after Blakeman's death. Other towns such as Cambria, New York (now Lockport, New York) were founded or expanded around new churches by Stratford descendants taking part in the westward migration. U.S. President Gerald Ford is a descendant of one of the Stratford founding families, that led by William Judson.

In 1939, one of the world's first successful commercial helicopters was developed in Stratford by Igor Sikorsky and flown at his plant. His company, Sikorsky Aircraft Corporation is still the town's largest taxpayer. Also in 1939, Lycoming produced Wright radial engines here. After WWII, the plant was converted to produce turbines.

Stratford, Connecticut once had a thriving theater, the American Shakespeare Festival Theater; it opened in 1955. Some of the world's biggest stars performed on this stage including Katharine Hepburn, Jessica Tandy, Nina Foch, and Hal Holbrook. John Houseman served as its artistic director during the late 1950s.

The Town of Stratford received the deed for the Stratford Festival Shakespeare Theater on February 8th 2005 from the State of Connecticut. On May 10, 2006 the town selected a New York City development company, Koerner Kronenfeld Partners LLC, to reopen the theater as a worldwide tourist destination. A limited 2006 summer season was scheduled for 2006.

Stratford is also home to one of the most successful women's softball teams in history, the Brakettes. They have won 24 national championships, including a record eight consecutive titles, from 1971 to 1978. Formed in 1949 as the Raybestos Girl All-Stars, and later the Raybestos Brakettes, they ceased being sponsored by Raybestos in 1985 and since then have been known as the Stratford Brakettes. Their most recent title came in 2004, capping another three-peat (titles in 2002, 2003, and 2004).[2]

A small museum in the former Stratford railroad station (eastbound, or northern side of the tracks) at 2480 Main Street, the museum contains a photographic history of the helicopter and many models. The museum has free admission and is open Wednesdays through Sundays, 1 p.m. to 4 p.m., from Memorial Day through October.

Stratford is home to the Great Meadows Unit of the Stewart B. McKinney National Wildlife Refuge, which is adjacent to Sikorksy Airport.

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