In 1997, Cahill asked his parents to allow him to travel to England to play professionally; they allowed him to do so. He lived in Grays, Essex with family until he was signed by Millwall on a free transfer from Sydney United. He made his Millwall debut on 2 May 1998 against Bournemouth at The Den, which Millwall lost 2–1. Cahill helped Millwall reach the 1999 Football League Trophy Final where they lost to Wigan Athletic.

He was part of the Millwall side that won the Football League Second Division championship with a club record 93 points in the 2000–01 season. He also reached two play-off semi-finals with Millwall in 2000 and 2002. Cahill was a central part of Millwall’s run to the 2004 FA Cup Final, their first appearance in the showpiece in club history, scoring the winning goal in the semi-final against Sunderland, and securing a UEFA Cup place in the process. Cahill polled over 100,000 votes to win the FA Cup “Player of the Round” award for his performance during the semi-final victory. His last game for the club was against Manchester United in the final, which Millwall lost 3–0. Cahill made 249 overall appearances for The Lions, scoring 56 goals in the process.

In February 2002, Cahill received an offer to play for the Republic of Ireland at the 2002 FIFA World Cup by Mick McCarthy, his former manager at Millwall. Cahill has Irish grandparents and McCarthy had hoped that Cahill would be interested. However Cahill was not eligible as he was cap-tied to Samoa.

FIFA changed its eligibility rules in 2004, allowing players capped at junior levels to switch international allegiance, meaning that Cahill was then able to play for England, Ireland, Australia or Samoa. He chose to represent the country of his birth.

Cahill made his debut for Australia in a friendly against South Africa on 30 March 2004 at Loftus Road, London. He then participated at the 2004 Olympic Games.

In October 2006, Cahill was named as one of 50 nominees for the Ballon D’Or, becoming the first Everton player in 18 years to be nominated, and the only player on the list from an AFC nation. He missed much of the 2006–07 season with injuries to his knee and foot, but signed a five-year contract extension at the season’s end.

Cahill played in the 2006 FIFA World Cup and, in Australia’s opening group game against Japan, became the first ever Australian to score a World Cup goal. Scoring a second goal in the same game, he earned man of the match honours.

Cahill returned from injury partway through the 2007–08 season in the club’s first UEFA Cup Group match, a home match against Greek side Larissa on 25 October 2007, scoring from a diving header after 14 minutes in a 3–1 win. His extra time winner against Luton Town on 31 October in the League Cup, sent Everton into their first cup quarter-final in more than 5 years. His 100th league appearance for Everton came in a 1–1 draw against Sunderland. Due to injuries to all four of Everton’s senior strikers Cahill was employed as a makeshift forward during December 2008. In this role he scored a late equaliser in the Merseyside Derby, becoming the first player since Dixie Dean to score for Everton in three Anfield derbies. His 100th career goal was scored against Arsenal at Goodison on 28 January 2009.

Everton fans have given him the nickname “Tiny Tim” after the Charles Dickens character because he is slightly short and slim. He has made a corner flag goal celebration his “trademark”. The celebration, where Cahill pretends to trade punches with the corner flag while putting the Everton badge between his teeth, was first seen in the 2005–06 season. On 2 March 2008, Cahill controversially celebrated his goal in the 3–1 home victory of Portsmouth by crossing his wrists as if he had been handcuffed. This was in reference to the recent jailing of his brother, Sean; Cahill later apologised for the gesture. Cahill dedicated his winning goal in a Europa League game against BATE Borisov to the victims of the earthquake and tsunami in Samoa, miming rowing a canoe after scoring in the second half of the match in Belarus.

Cahill became involved with two football academies in 2009, one based in Wollongong, Australia in partnership with Wollongong Police and Community Youth Club, and another in partnership with ‘Elite Sporting Academy’ in Dubai.

Cahill scored two goals against Aston Villa on 14 April 2010 both coming from headers to move his goal tally for the season to nine goals all coming from his head. Three days later against Blackburn, Cahill scored a 90th-minute winner, to give Everton a 3–2 victory. Taking his tally to 10 goals that season.

Cahill made his 200th appearance for Everton on 25 April 2010 in a 2–1 against Fulham and signed a new four-year contract the following month. He scored his 5th goal in a Merseyside derby, in a 2–0 win over Liverpool in October 2010, and his 50th Premier League goal a month later, in a game against Blackpool. The Aussie received a foot injury during the 2011 Asia Cup finals which limited his appearances until the end of the season to only nine – eight league games and one in the FA Cup.

In 2010 Cahill married his childhood sweetheart Rebekah Greenhill in Las Vegas, en route to Sydney. The couple have four children, Kyah (son, born 2003), Shae (son, born 26 April 2005), Sienna (daughter, born 2007), and Cruz (son, born 2 September 2012). As of 2015, the Cahills owned homes in Sydney, Florida, New York, Shanghai, and England.

Following his participation in the 2011 Asian Cup, Cahill had the longest goal drought in his career. He scored his last league goal in December 2010 away to Manchester City and went the whole of 2011 without finding the net. The run stretched to 34 games, but was finally ended when he scored the opening goal, a tap in from close range, in a 1–1 draw with Blackburn Rovers in January 2012.

On 13 May 2012, during Everton’s last match against Newcastle United at Goodison Park, Cahill was sent off for violent conduct after the full-time whistle for an altercation with Yohan Cabaye.

In July 2012 Cahill signed for the New York Red Bulls of Major League Soccer as a Designated Player, for a fee reported to be approximately £1 million. He made his MLS debut in a game against the Houston Dynamo the following month. On 19 May 2013 Cahill scored a goal which turned out to be the winner in the 91st minute against the Los Angeles Galaxy in a 1–0 win. On 20 October 2013, Cahill set a new record (broken in 2015 by Mike Grella) for the fastest goal in MLS history when he scored eight seconds into a 3–0 win against the Houston Dynamo. Cahill replaced suspended forward Bradley Wright-Phillips in the second leg of the Red Bulls’ MLS Cup semi-final against the New England Revolution on 29 November 2014. Despite Cahill opening the scoring in the 26th minute to level the tie, the Red Bulls bowed out with a 2–2 draw in Massachusetts, losing 4–3 on aggregate. On 2 February 2015, Cahill left New York Red Bulls by mutual agreement.

On 5 March 2014, in a pre-World Cup friendly match against Ecuador, Cahill became Australia’s all-time top goalscorer with 31 goals, scoring twice in a 4–3 loss.

Cahill scored Australia’s only goal in their opening group match against Chile on 13 June 2014. He joined Portuguese star Cristiano Ronaldo, Mexican defender Rafael Márquez, Dutch players Robin van Persie and Arjen Robben, German player Miroslav Klose, and American Clint Dempsey as the only players to score at the 2006, 2010 and 2014 FIFA World Cups.

Cahill’s business career is diverse across a range of industries. BRW quoted his net worth to be $28 million in 2014.

Following his departure from New York Red Bulls, Cahill signed with Chinese club Shanghai Shenhua. On 9 March 2015, Cahill debuted for Shanghai Shenhua in the team’s opening game of the 2015 Chinese Super League season, a 6–2 win over rivals Shanghai Shenxin. Shanghai Shenhua also went to the Chinese FA Cup final in which they were defeated by Jiangsu Sainty after extra time.

Tim Cahill was selected under manager Ange Postecoglou as part of his squad which competed in the 2015 AFC Asian Cup. A campaign in which Australia was the host nation with matches hosted across four cities including Canberra, Brisbane, Melbourne and Newcastle, Cahill competed well in what became his nation’s inaugural Asian Cup title. He scored three goals in the tournament.

On 16 February 2016, Cahill announced on social media that he had terminated his contract with Shanghai by mutual agreement upon being told that he was not part of new coach Gregorio Manzano’s plans for the 2016 Chinese Super League season.

On 22 February 2016, it was reported that Cahill signed with Chinese Super League club Hangzhou Greentown. On 6 March 2016, Cahill scored a penalty on his Hangzhou Greentown debut in a 2–1 win against Changchun Yatai. Cahill decided to come back to Australia for his family in the summer of 2016. On 14 July 2016, he had his contract terminated by mutual consent.

On 11 August 2016, Cahill signed a three-year contract with A-League club Melbourne City, with the plan to play the first two years and then take on a coaching role for the third year. Cahill made his debut in the FFA Cup on 24 August as a 64th-minute substitute against Brisbane Strikers. In his second game for Melbourne City he scored and got an assist in a 4–1 win in the FFA Cup quarter final against Western Sydney Wanderers. Cahill made his A-League debut in a Melbourne Derby against Melbourne Victory on 15 October 2016. He opened the scoring with a spectacular volley into the top corner from 35 metres out after 27 minutes. City won the match 4–1. On 30 November 2016, Cahill scored a trademark header in the FFA Cup Final. The victory over Sydney FC was the club’s first piece of silverware.

Cahill was chosen to start against Jordan in a top-of-the-group clash, in which he notched a brace on 29 March 2016. Cahill scored the winning goal for the Socceroos against the United Arab Emirates in a 1–0 away victory. He helped Australia reach the inter-confederation play-offs by scoring two goals, including the winning goal in the second half of extra time in their 2–1 second leg victory against Syria (3–2 on aggregate). On 15 November 2017, he started in the 3–1 win over Honduras which saw Australia clinch a spot in the 2018 FIFA World Cup.

On 4 February 2017, just as he was preparing to come on as a substitute against Melbourne Victory FC, Cahill was sent off for using “insulting, offensive, abusive language towards a match official” after he angrily disputed a goal with Chris Beath. This is the first time in Australian football history in which a player was sent off before entering the field of play.

On 6 December 2017, Cahill left Melbourne City after not getting enough game time, in a bid for more game time at club level to boost his chances to get selected for the Australian squad for the 2018 FIFA World Cup.

On 29 January 2018, Cahill re-joined his first professional club, Millwall, signing until the end of the 2017–18 EFL Championship season. A week after his return, he played for Millwall’s under-23 team in the Professional Development League scoring a goal in their 3–2 victory over Coventry City. The following week, Cahill made his second Millwall debut, coming on in the 90th minute to a standing ovation.

On 1 September 2018, Cahill signed with Indian Super League club Jamshedpur FC. However, he could not make his debut in the first game of the season against Mumbai City FC due to suspension in the game. Cahill also scored for the club and played couple of matches in ISL.

In May 2018, Cahill was named in the World Cup squad by coach Bert van Marwijk and made a single appearance in the tournament, coming off the bench in the 63rd minute of the 2–0 loss against Peru.

On 16 July 2018, Cahill announced his retirement from international football, subsequently overturned with the decision to participate in one final home friendly against Lebanon in November 2018. He retired with 50 goals (a national team record) in 108 games (the second highest, and just three behind Mark Schwarzer).

On 28 March 2019, Cahill announced his retirement from football.

Cahill was officially announced as an ambassador for Australia’s Securities Broker ACY Securities on 30 October 2019.