After an unbeaten run of seven games, Gillingham were fourth in the league table in late September, just outside the top three places which would result in promotion to the Second Division.

Ron Hillyard, Mel Sage, and Karl Elsey made the most appearances; all three played in all 58 of the team's competitive games.

The highest attendance recorded at the club's home ground, Priestfield Stadium, was 8,983 for an FA Cup game against Derby County in January.

Karl Elsey, a midfielder, arrived from Cardiff City on a free transfer and David Byrne, a winger, joined the club from semi-professional team Kingstonian of the Isthmian League.

[7] During the break between seasons, the club spent £80,000 (equivalent to £310,000 in 2023) installing new executive boxes within Priestfield Stadium's main stand.

Work also needed to be undertaken to satisfy new safety requirements following the Bradford City stadium fire two months earlier.

This was not completed in time for the club's first friendly match of the pre-season, against Queens Park Rangers, which was therefore played behind closed doors.

[9] The team's first game of the Third Division season was away to Lincoln City on 17 August;[10] Elsey made his debut in the starting line-up.

[13] Two days later, Gillingham won their first league game of the season, defeating Bristol City 2–1 away from home with two goals from Tony Cascarino, and ended August by beating Bolton Wanderers by the same score at Priestfield.

[16] The team won consecutive games in mid-October against Cardiff City and AFC Bournemouth before losing 2–1 at Priestfield against fellow promotion contenders Derby County.

[19] The team were undefeated in five league games in November, including three consecutive victories in which they scored a total of 12 goals.

[20] The unbeaten run ended with a 1–0 defeat away to Bristol Rovers on 14 December and Gillingham then lost 3–2 away to Darlington six days later.

David Tong, a midfielder, joined the club from Bristol City on a short-term contract until the end of the season and Dale Tempest, a forward, arrived on a one-month loan from Huddersfield Town.

[11] Tempest scored two goals in a 3–0 victory which made Gillingham the only team of the season to defeat the eventual Third Division champions both at home and away.

[10] Commenting on the match against Derby, Simon O'Hagan of The Times wrote that Gillingham, who could normally be "dangerously inventive", were hampered by terrible weather conditions.

Gillingham entered the 1985–86 Football League Cup in the first round, being drawn against Southend United of the Fourth Division.

The higher-level team won 3–1 at Priestfield in the first leg and 2–1 at their own Fratton Park ground in the second to eliminate Gillingham from the competition by an aggregate score of 5–2.

The 1985–86 Associate Members' Cup, a tournament exclusively for Third and Fourth Division teams, began with a preliminary round in which the teams were drawn into groups of three, contested on a round-robin basis; Gillingham's group also contained fellow Third Division sides Derby County and Brentford.

[55] Gillingham's next opponents were Cambridge United of the Fourth Division; the game, held at Priestfield on 24 January, again drew an attendance of less than 2,000.

[56] The southern section semi-final did not take place until April and paired Gillingham with fellow Third Division side Bristol City.

[57] Hinnigan was sent off for a foul on Steve Neville, which assistant manager Taylor described in his next programme notes as "totally unjust",[58] and the game ended 3–0 to Bristol City, ending Gillingham's participation in the tournament; Bristol City went on to win the Associate Members' Cup final at Wembley Stadium.

[63] FW = Forward, MF = Midfielder, GK = Goalkeeper, DF = Defender Cascarino was voted into the Professional Footballers' Association Team of the Year for the Third Division by his fellow professionals, the second consecutive season in which he had been honoured and the fifth consecutive season in which a Gillingham player had been selected.