During its 11 seasons in the ESFL, Box Hill only failed to qualify for the grand final on 3 occasions – 1938, 1940 (when the club withdrew mid-season) and 1950.

Success did not come readily at first as the team largely based on its ESFL players and local juniors struggled to make the transition to senior football.

Improvement was steady during the early VFA years and the appointment of former Richmond champion and 1948 Brownlow Medallist Bill Morris as playing coach for the 1952 season proved to be an excellent choice.

Morris played with Box Hill for three years and won the best and fairest by a huge margin each season and must still be regarded as one of the very best players ever to represent the club.

When divisional football was introduced for the 1961 season Box Hill therefore became the final club admitted to the newly formed ten team first division.

Divisional football was conducted in the VFA for 28 years from 1961 to 1988 and Box Hill played a total of 24 seasons in the second division (1962 to 1984, 1986).

Box Hill did not gain Council's permission to play Sunday matches on its own ground until 1969, the final VFA club to do so.

Through the 1960s, the club relied on a successful Saturday night dance that it hosted at the Box Hill Town Hall for most of its income.

Box Hill's improved form during 1969 was the launching place for a successful 1970 season in which it played Coburg in its first VFA grand final.

Its opponent Coburg had lost only twice during the course of the season but both of these losses were to Box Hill and the Mustangs were therefore given a good chance of winning promotion.

Box Hill's financial position was stabilised in 1981 and thereafter the club's on-field performances improved rapidly culminating in an outstanding 1984 season in which Box Hill claimed its first VFA premiership in overwhelming fashion, losing only two games for the season and achieving the highest ever score and greatest winning margin ever recorded in a VFA grand final in defeating Oakleigh by 135 points, 32.23(215) to 11.14(80).

In 1989 former Carlton premiership player Peter Francis guided the club to 3rd place, equalling its best VFA result to that time.

In 1994 Box Hill finished 2nd on the ladder and reached its first major VFA grand final under the coaching of John Murphy.

Box Hill established a 24-point lead at 3/4 time against the more favoured Sandringham team but was overrun in the final quarter, losing narrowly 10.9(69) to 11.12(78).

After a period of some uncertainty, all 9 remaining VFA clubs, along with North Ballarat and Traralgon were granted licences for the first season of the new VFL competition in 1996.

Box Hill's results in the initial VFL years between 1996 and 1999 showed a club which remained competitive but not able to win enough games to qualify for the Finals.

Due to the complexities involved in finalising the details of such an arrangement, only 3 AFL clubs participated in an "alignment" partnership in the VFL in 2000.

On 23 December 1999, Box Hill and Hawthorn created one of the first such partnerships, considered to be one of the more natural and logical of such arrangements, due to such factors as both clubs wearing brown and gold playing uniforms and Box Hill being geographically located within the heartland of Hawthorn's membership and supporter base.

Such was the case for the Box Hill Hawks, which between 2000 and 2005 completed the most successful period of its long history, with 6 consecutive finals appearances.

After finishing the home-and-away season in 2nd place with 15 wins and 5 losses, it defeated Springvale and the Murray Kangaroos to claim a grand final berth against Werribee.

The Box Hill Hawks again played in the grand final in 2003 under the coaching of former Western Bulldogs champion and 1990 Brownlow Medallist Tony Liberatore.

Wiliamstown, at that time aligned to Collingwood, fielded an unprecedented 16 AFL listed players in its grand final team and proved too strong for the Box Hill Hawks, which fought hard after it trailed by more than seven goals at half-time; Wiliamstown eventually prevailed by 29 points 13.14(92) to the Box Hill Hawks 9.9(63).

Following a large turn-over of players after the 2003 grand final defeat, Box Hill lost the opening 6 games of the 2004 season under new coach Andy Collins and after 9 rounds was still last on the ladder with just 1 win.

It defeated Geelong in the First Elimination Final before narrowly losing an epic semi-final to Port Melbourne 19.10(124) to 19.14 (128) in a game rated as one of the best played in the VFL for many years.

In circumstances uncannily reminiscent of the previous season, the Box Hill Hawks won its Elimination Final in strong fashion and again met Port Melbourne in the First Semi-final.

In 2023, following Hawthorn's ascension to the AFL Women's competition, the VFLW license was returned to Box Hill, and the club has played under that name in the league ever since.

The white horse emblem was added prior to the 1938 season, coinciding with the club's move from Surrey Park to Box Hill City Oval.