Lennon joined Glenavon, after reaching the final of the Milk Cup with Glenavon Select and scored on his Irish League debut. He then joined Manchester City as a trainee in 1987. He made one first team appearance during his time in Manchester, a league match on 30 April 1988 away against Birmingham City, before signing for Crewe Alexandra on a free transfer in August 1990. Lennon made his debut for Crewe on 18 September 1990 against Reading. Despite missing the whole of season 1991–92 due to a back injury, he became an established member of the side and impressed with his intelligent play and consistent performances. Lennon’s form saw him make his debut for Northern Ireland in 1994, and thus became the first Crewe Alexandra player in 60 years to win a full international cap. In 5½ years at Crewe, Lennon made 187 appearances for the club and scored 18 goals.

Lennon made his international debut for Northern Ireland on 11 June 1994 when he come on as a substitute in a friendly against Mexico in Miami. He had to wait nearly a year for his next cap when he played against Chile in another friendly. Lennon made his first competitive appearance three months later on 3 September 1995 in a European Championship qualifier away against Portugal. After that, Lennon became a fixture in the international side although Northern Ireland were unsuccessful in their attempts to qualify for the finals of major tournaments.

In February 1996, Lennon signed for Leicester City for a fee of £750,000. In May 1996, Lennon played in the Leicester City side that defeated Crystal Palace 2–1 at Wembley in the Play-off Final to win promotion to the Premier League. On 16 April 1997, Lennon picked up his first major winner’s medal when Leicester won 1–0 against Middlesbrough in a replayed League Cup Final. He played in a further two League Cup Finals during his time at Filbert Street, losing 1-0 to Tottenham Hotspur in March 1999 but winning 2–1 against Tranmere Rovers in February 2000.

An on-field incident during a league match in 1998 against Newcastle United between Lennon and Alan Shearer resulted in the England international being charged with misconduct by the FA, Television footage showed Shearer appearing to intentionally kick Lennon in the head following a challenge. The referee of the game took no action against Shearer. Shearer apologised afterwards, but denied that the contact with Lennon was deliberate, and Lennon later gave evidence in Shearer’s defence at the FA hearing which subsequently cleared the Newcastle and England striker of all charges.

After Martin O’Neill became the new manager of Celtic in June 2000, he made several attempts to sign Lennon. Finally after months of protracted negotiations with Leicester, on 6 December 2000 Lennon joined the club he supported as a boy for a fee of £5.75 million. That season saw Lennon pick-up three winner’s medals as Celtic swept to a domestic treble, winning the Scottish Premier League, Scottish Cup and Scottish League Cup. The next four seasons at Celtic saw Lennon win a further two league championships and two Scottish Cups. He was also an integral part of the Celtic side that reached the UEFA Cup Final in 2003, losing 3-2 to Porto after extra time.

Lennon decided to retire from international football in August 2002 upon receiving a death threat before a Northern Ireland match against Cyprus. The threats came after his alleged claim that he wanted to play for a team representing a United Ireland. The threat was allegedly made by the Loyalist Volunteer Force, although the organisation later denied this.

When Gordon Strachan took over from Martin O’Neill as Celtic manager in the summer of 2005, he made Lennon Celtic captain. In January 2006 when his former club Leicester City sacked Craig Levein, Lennon was linked with a return to the Midlands side in a player-manager role. He went on record saying he was flattered but wanted to captain Celtic to the Scottish Premier League title.

Although he was also linked with a move to Crystal Palace in a player-manager role in the summer of 2006, on 23 June 2006, Celtic announced he had signed a new one-year contract. Sunderland manager Roy Keane made an attempt to sign Lennon prior to the closure of the August 2006 transfer window, but his approach for the player was rejected by Celtic. On 25 April 2007, Lennon announced he would be leaving Celtic, and in his last game for the club on 26 May 2007, he captained the team to victory in the Scottish Cup Final against Dunfermline Athletic. Celtic’s 1–0 win clinched the League and Cup Double.

Lennon joined League One club Nottingham Forest on a one-year contract with an option for a second year on 12 June 2007. He made his debut captaining the side in a 0–0 draw at home to Bournemouth. He missed a week’s training with Forest in November 2007, because of family reasons in Scotland, and lost his place in the team as a consequence.

Lennon joined Wycombe Wanderers of League Two on a free transfer on 31 January 2008, managed by his former Celtic midfield partner Paul Lambert. He left on 3 April to take up a coaching role with Celtic.

Lennon was linked with the vacant manager’s job at Hibernian after the resignation of John Collins, but the job was given to Mixu Paatelainen. Lennon’s first coaching appointment was as first team coach with Celtic in 2008. After the appointment of Tony Mowbray as Celtic manager, Lennon took charge of the Celtic reserve team.

Following Mowbray’s departure from Celtic on 25 March 2010, Lennon was appointed caretaker manager for the remainder of the 2009–10 season. He appointed former teammate Johan Mjällby as his assistant. Celtic won all of their remaining league games under Lennon, including wins over Kilmarnock, Hibernian, and Rangers, but lost 2–0 to First Division side Ross County in the semi-final of the Scottish Cup. In the aftermath of that defeat, Lennon spoke frankly about the Celtic players and their performances over the course of the season. He said that they had lacked “hunger and desire” and that whether he was installed as manager or not, he would be recommending a significant clear-out of players to the board.

Lennon was appointed manager of Celtic on a full-time basis on 9 June 2010. He retained Mjällby as his assistant, as well as former Celtic teammate Alan Thompson and former Leicester City teammate Garry Parker as first-team coaches

On 28 July, in his first competitive game as full-time manager, Celtic lost 3–0 away to Braga in the UEFA Champions League. Celtic won their first eight league matches under Lennon, although controversy erupted in their 2–1 win away at Dundee United on 17 October 2010. Celtic were awarded a penalty kick in the second half, but the decision was then rescinded by referee Dougie McDonald. McDonald explained after the match that he over-ruled the penalty award on the advice of the assistant referee. Lennon reluctantly accepted McDonald’s explanation, commenting “I suppose you have to put it down to another honest mistake by the referee.” It was, however, later revealed that McDonald had lied in his explanation over the penalty award and the referee subsequently resigned several weeks later having received a warning from the Scottish Football Association after failing to properly explain his overturning of the penalty award. Further referring controversy ensued the following week when Celtic lost their unbeaten run in the league, losing 3–1 at home against Rangers. The Ibrox club’s third goal came as a result of penalty awarded when Rangers’ Kirk Broadfoot fell to the ground under a challenge from Celtic’s Daniel Majstorović. Broadfoot appeared to have dived, and television footage showed that the referee had his back to the play when the challenge occurred, only turning in time to see Broadfoot fall to the ground. Lennon stated afterwards that he felt the referee “got a couple of decisions wrong”, and added regarding the penalty, “I’m not sure that he saw it so I don’t know why he’s given it. He’s got a lot of questions to answer”. In November, Lennon led Celtic to a 9–0 win over Aberdeen, a record win in the Scottish Premier League and Aberdeen’s heaviest ever defeat. Celtic lost their next game 2–0 away against Hearts, with Celtic’s Joe Ledley sent off for the first time in his career for a “strong” challenge on Ian Black. Celtic were later denied a penalty award in the second half, and shortly afterwards Lennon was sent to the stand by the referee. Lennon defended Ledley after the match, describing referee Craig Thomson’s decision as “ridiculous”. Lennon was later given a six match touchline ban for excessive misconduct as a result of the incident in the Hearts’ game, although it was later reduced to four matches after appeal. He was given another four match touchline ban by the SFA following an altercation with Rangers assistant manager Ally McCoist after a Scottish Cup match in March 2011.

Lennon led Celtic to the final of the League Cup in March 2011, but they lost 2–1 to Rangers after extra time. They remained in contention for the SPL title until the final day of the 2010–11 season, when they won 4–0 at home to Motherwell, but finished a point behind Rangers. He won his first silverware as a manager when Celtic beat Motherwell 3–0 in the Scottish Cup Final a week later.

In January 2011, Lennon reached an out of court settlement with the Bank of Ireland after a company of which he was a director defaulted on a 3.7 million euro loan.

After rallying from a poor start to season 2011–12, Lennon won the SPL Manager of the Month award for November 2011. The club went on to win the 2011–12 Scottish Premier League and Lennon was made SFWA Manager of the Year. Lennon then guided Celtic through two qualification rounds to reach the group stage of the 2012–13 UEFA Champions League, where Celtic beat Barcelona one day after the club’s 125th birthday. Celtic qualified out of their group to the knock-out stages of the Champions League. Celtic were comfortably beaten on aggregate by Juventus in the last 16 round, but both Celtic and Lennon were still praised for their overall Champions League campaign. On 21 April 2013, Celtic retained the Premier League title. Lennon finished the season by leading Celtic to a League and Cup double with a 3–0 win over Hibernian in the Scottish Cup Final.

Celtic qualified for the group stages of the Champions League again the following season, but had a dismal campaign; winning only once with a 2–1 home win over Ajax, and slumping to a 6–1 rout away against Barcelona in the final group match. They fared little better in the domestic cup competitions; losing 1-0 to Morton in their first game in the Scottish League Cup, and losing 2-1 to Aberdeen in the fourth round of the Scottish Cup. The League campaign was much more impressive through; undefeated until February and losing only twice in all over the course of the season in which they scored 102 goals on the way to their third successive League title. On 22 May 2014, Lennon announced that he was leaving Celtic after four years as manager. “I have parted company with Celtic,” he said in a brief statement, adding “The club are in a very strong position and I wish the fans and the club all the very best for the future.”

Lennon was announced as the new manager of Bolton Wanderers on 12 October 2014, signing a four-year contract. He won his first game in charge 1–0 against Birmingham City at St Andrew’s stadium, although he was sent to the stands in the 81st minute after an altercation with referee Mark Hayward caused by Lennon leaving his technical area before Craig Davies’s penalty was saved. Lennon’s first three months in charge saw Bolton rise ten places from bottom of the league up to fourteenth; a spell that included an eight match unbeaten run and four consecutive clean sheets. Bolton reached the fourth round of the FA Cup and took Liverpool to a replay before conceding a last minute goal to lose 2–1 and go out. Things didn’t go well for Lennon thereafter, with Bolton winning only one of their last 11 games of the season, and Barry Bannan and Neil Danns being suspended by Lennon for off-field indiscipline. Bolton did however succeed in avoiding relegation, finishing 18th in the league.

Bolton struggled at the start of the following season, and by October 2015 were lying bottom of the table with only one win in their first eleven league games. Lennon maintained confidence in his ability to improve Bolton’s fortunes, stating “I didn’t realise quite how tough it was going to be but I have got faith in my own ability and I believe we’ll turn things around.” By the end of November 2015, Bolton had gone on a run of twelve games without a win, and remained bottom of the Championship. At this time, the club announced that their squad had not been paid this month “due to a short-term funding issue” in a statement which came hours before their 1–1 draw with Brentford. In that game, Bolton striker Gary Madine was seen on television mouthing an insult towards Lennon, although the manager played down the incident afterwards, stating “I don’t know what he said. He’s a Geordie, I can’t understand him! It was probably reciprocated!” Bolton continued to struggle and, with the club at the bottom of the table, Lennon left by “mutual consent” on 15 March 2016.

Lennon was appointed head coach of Scottish Championship club Hibernian in June 2016. He led the “Hibees” to the Scottish Championship title and promotion back to the Scottish Premiership (after a three-season absence) in his first season. In September 2017, Lennon and Hibs agreed to extend his contract to the end of the 2019–20 season. Hibs finished fourth in the 2017–18 Scottish Premiership and qualified for the Europa League.

On 25 January 2019, Lennon was suspended by Hibernian following an exchange with other club employees. On 30 January, it was announced that he and assistant coach Garry Parker had left the club by mutual consent. A club statement said that “neither Neil nor Garry has been guilty of any misconduct or wrongdoing and no disciplinary process has been commenced. The suspension, put in place to allow an internal review, was lifted by the club as part of this agreement.”

On 26 February 2019, Lennon was appointed manager of Celtic until the end of the season, after Brendan Rodgers moved to Leicester City. Having helped the club achieve an unprecedented third domestic treble (“treble treble”), Lennon was appointed permanent manager for a second time.