In the late 1930s, Larry Floyd and Bill Dooley decided to adopt a more modern nickname, and the club became formally known as "the Seagulls".

As a result of skilful management by such officials as secretary Larry Floyd, president Bill Dooley and treasurer Jim McConville,[4] plus the termination of contract agreements with the VFL, Williamstown recruited Harry Vallence, a star goal-kicker from Carlton, plus Gordon Ogden and Eric Glass from Melbourne for the 1939 season.

Following the end of the throw-pass era in 1950, many Association clubs began to struggle through the following decade as the prestige of the VFA declined.

[6] Under Carter, the club won three consecutive premierships in 1954, 1955 and 1956, and was unbeaten in the 1957 home-and-away season before losing two semi-finals and finishing third.

The club reached five grand finals between 1985 and 1990: it lost the 1985 decider by one goal to Sandringham, won the 1986 premiership against Coburg under Wheeler, lost consecutive grand finals against Coburg in 1988 and 1989, then defeated Springvale to win the 1990 premiership under captain-coach Barry Round.

At the end of the 1995 season, the club's survival was threatened when the Victorian State Football League sought to align the VFA (which at that time renamed the VFL) with the TAC Cup, and needed only one western suburban team to align with the Western Jets; as such, it ordered Williamstown to merge with Werribee.

[16] After the clubs could not agree to terms, the VSFL decided to grant the remaining licence and the affiliation with the Jets to Williamstown, resulting in Werribee's temporary expulsion from the VFL.

[21] Year Captains Coaches Gerry Callahan Medalists Williamstown also holds the record for the highest ever score in Australian rules football, in any league and at any grade, with a 675 point win over Geelong West in a 1983 thirds division match.

The Williamstown Football Club's guernsey consists of a royal blue background with a diagonal yellow sash.