It competed in the Conference Premier (now the National League) during the 2006–07 season under the guidance of the then chairman and Manager Colin Lippiat, but was relegated back to the Conference South after one season and subsequently suffered a further relegation in 2010–11, before returning to the sixth tier in 2013–14 after beating Chesham United 3–1 in the play-off final.

[7] St Albans were semi-finalists in the 1998–99 FA Trophy, losing 4–3 over two legs to Forest Green Rovers.

In Summer 2009, it was announced that Gibson's building firm, William Verry, were to go into administration with debts mounting continuously.

The punishment was handed down to City chairman John Gibson and then vice-chairman Alasdair McMillin during a Regulatory Hearing at the Association's offices at Wembley, and was in relation to alleged illegal payments to players, described by the FA as financial irregularities, by the club during the 2008–09 season.

Now playing in the Southern League Premier Division for the first time in their history and at their lowest level for over 20 years, the saints finished 8th.

[2] They reached the first round of the FA Cup in the 2016–17 season, meeting League Two side Carlisle United but lost 5–3 at home.

[2] They beat League Two leaders Forest Green Rovers in the first round but lost to Hertfordshire rivals Boreham Wood in the second.

[2] Following the end of the season David Noble was bought back as Head Coach with Meakes returning to his position as assistant[16] Rock band, Enter Shikari, who are from St Albans, have been the main sponsor of St Albans City Football Club since 2020.

[17] Note: Flags indicate national team as defined under FIFA eligibility rules; some limited exceptions apply.

Note: Flags indicate national team as defined under FIFA eligibility rules; some limited exceptions apply.