[18] During this time, the club embarked on one of the most notable runs in FA Cup history, as manager Dick Graham took his ageing side to the 1970–71 quarter-finals, dispatching non-league Ringmer, Cambridge United, Barnet and Rochdale following a replay.

With the draw having been made prior to the replay against Rochdale, the U's knew they would face a home tie with First Division Leeds United, and duly trounced Dale 5–0.

In the match with Leeds, the U's raced to an unprecedented 3–0 lead in front of a 16,000 Layer Road crowd, with two goals from Ray Crawford and one from Dave Simmons.

[20] Despite a brief turn around in form under former Rangers manager Jock Wallace,[21] United were relegated from the Football League for the first time since their election.

[22] The club had a successful 1995–96 season as they reached the 1995–96 Football League play-offs, but were defeated by Plymouth Argyle at the semi-final stage.

[22] The club narrowly missed the play-offs in 1996–97[25] but did however reach the Football League Trophy Final held at Wembley.

However, when Parkinson left to take the reins at Hull City, his assistant Geraint Williams was handed the daunting task of guiding Colchester into their first season in the Championship.

[22] During the club's second season in the Championship, Layer Road hosted its final game on 26 April 2008 as the U's fell to a 1–0 defeat to Stoke City.

The club then moved to their new ground, the Colchester Community Stadium, in the summer of 2008 in preparation for life back in the third tier.

[22] The game saw a record crowd of 10,064 watch as the U's fell to a 5–0 defeat, with Ian Henderson being sent off on his United debut against his former club.

[37] Colchester secured League One safety on the final day of the 2014–15 season when they beat promotion hopefuls Preston North End 1–0 on 3 May 2015.

[38] However, Colchester could not stave off relegation to League Two in the 2015–16 season as they finished the campaign in 23rd position, confining them to the fourth tier of English football for the first time in 18 years.

The coat of arms, which features the living cross of St Helena and the crowns of the Three Kings, was used until 1972, when a dispute between the club and Colchester Borough Council pushed United to design a new crest.

Primary shirt sponsorships have included Royal London Group (1980–1986),[44] 0800 Linkline (1986–1987),[42] Norcross Estates (1987–1990), Holimarine (1990–1991), Colchester Hippodrome (1991–1992), The Sun (1992, 1992–1993), Strovers (1993–1994), SGR Colchester (1994–1996), Goldstar Fabrications (1996–1997), Guardian Direct (1997–1999), East Anglian Daily Times (1999–2000), JobServe (2000–2002, 2018–2019), Tiptree Jams (2002–2004), ICS Triplex (2004–2005), Easy-Skip (2005–2006), MutualPoints.com (2006–2007), Haart (2007–2008), Weston Homes (2008–2010, 2013–2018), ROL Cruise (2010–2012), TEXO Scaffolding (2019–2022), Workhorse Group (2022-2024) and HotLizard Ltd (2024-Present).

Away shirt sponsorship has been provided by Ashby's (1999–2000), Ridley's (2000–2002), 188Trades.com (2005–2006), Smart Energy (2006–2009), JobServe (2009–2010, 2012–2020), Strikerz Inc. (2020–2021), Workhorse Group (2021-2024) and HotLizard Ltd (2024-Present).

The U's shared the facilities with Town, as Colchester United's first ever game at the ground came on 2 September 1937, a 6–1 win against Bath City.

This was followed by the outbreak of World War II, and Layer Road was closed down by the club and passed over to Colchester Garrison.

[5] The ground hosted the record home crowd for a Colchester United game on 27 November 1948 for an FA Cup first round tie with Reading.

In 1980, the club's chairman Maurice Cadman announced that Layer Road was in need of £280,000 of basic safety improvement to meet legislation.

[56] The club played their final match at Layer Road in front of 6,300 on 26 April 2008 as they fell to a 1–0 defeat to Stoke City.

[57] Colchester United hosted the opening ramp-up event to Spanish club Athletic Bilbao on 4 August 2008.

[58][59] The first competitive fixture at the Community Stadium came on 16 August 2008 when Colchester hosted Huddersfield Town in front of a crowd of 5,340.

[71] The club also contest the Pride of Anglia award, which they have won once when they finished in 10th position in the Championship ahead of East Anglian rivals Ipswich Town and Norwich City.

[78][79] Colchester United's widest margin victory in the league was a 9–1 win over Bradford City on 30 December 1961 at Layer Road.

[80] The club's record home attendance was for an FA Cup first round tie at Layer Road with Reading on 27 November 1948, when 19,072 fans turned up for a game that was abandoned after 35 minutes due to thick fog.

[32] The highest transfer fee received for a Colchester United player is £2,500,000 for Greg Halford by Reading in January 2007.

[81] The highest fee paid by Colchester United for a player was £400,000 for Cheltenham Town striker Steven Gillespie in the summer of 2008.

At the end of the 2006–07 season, Colchester United created a "Hall of Fame", with inducted players being one of "those who have made a difference to the club's history".

[87] New inductees have been announced most seasons since 2007, with the entire team that famously defeated Leeds United in the FA Cup in 1971 entered into the Hall of Fame.

[90] In addition to the Hall of Fame, which excludes players who are currently active, Lomana LuaLua was named as Colchester United's cult hero by fans in a poll by the BBC in 2004, with the Congolese international registering 39% of the overall vote.