In an interview with BBC Sport he said, “As far as I can remember, we used to play with anything, with any round thing we could find, and whenever we managed to get hold of a ball, that was a bonus! I mean it was amazing!” In 1990, he joined Enugu Rangers. In his time at the club he produced many spectacular displays including one where he rounded off and scored a goal, against experienced Nigerian goalkeeper Willy Okpara in a match against BCC Lions. Later that year, he went on holiday to West Germany, the country that had just won the 1990 FIFA World Cup, so he could watch German league football. His friend Binebi Numa was playing in the Third Division for Borussia Neunkirchen, and one morning Okocha accompanied Numa to training, where he asked to join in. The Neunkirchen coach was impressed with Okocha’s skills and invited him back the next day before offering him a contract. A year later, he joined 1. FC Saarbrücken, but stayed only a few months with the 2. Bundesliga side before a move to the 1. Bundesliga with Eintracht Frankfurt.

Okocha joined Eintracht Frankfurt in December 1991, where he linked up with many well-known players including Ghanaian international striker Tony Yeboah and later Thomas Doll. He continued to shine for the German side, one highlight being a goal he scored against Karlsruher SC, dribbling in the penalty box and slotting the ball past goalkeeper Oliver Kahn even going past some players twice. The goal was voted Goal of the Season by many football magazines, and also voted as 1993 Goal of the Year by viewers of Sportschau (an ARD German TV sports programme). In 1995, Okocha, Yeboah and Maurizio Gaudino were all involved in a feud with manager Jupp Heynckes, which led to their departure from the club.

Okocha made his official debut for Nigeria in their 2–1 1994 FIFA World Cup Qualifier away loss against Ivory Coast in May 1993. It was not until his second cap and home debut that he became a favourite with the Nigerian supporters. With Nigeria trailing 1–0 against Algeria, in a match they needed to win, he scored from a direct free kick to equalise, before helping the team to a 4–1 win, eventually securing qualification to their first World Cup. In 1994, he was a member of both the victorious 1994 African Cup of Nations squad. And the World Cup squad who made it to the second round before they lost in a dramatic match against eventual runners-up Italy.

In 1996, Okocha became a key member of an arguably more successful Nigerian side, their Olympic gold winning side at the Atlanta Games, later nicknamed the Dream Team by the Nigerian press after the USA 1992 Olympic gold winning basketball team. In the 1998 FIFA World Cup hosted by France, Okocha played for a disappointing Super Eagles side who failed to live up to expectations again reaching the round of 16, albeit with less impressive performances save for their 3–2 opening win against Spain. This did not destroy interest in Okocha, who had entertained fans with his trademark skills and dribbles and went on to be named in the squad of the tournament.

In 1998, French side Paris Saint-Germain spent around £14 million to sign Okocha, making him the most expensive African player at the time. During his four-year stint with PSG, he played 84 matches and scored 12 goals. He has also served as a mentor, at the time, for young Brazilian footballer Ronaldinho during his time in Paris.

Okocha again joined the Super Eagles in the 2000 African Cup of Nations co-hosted with Ghana. He scored three goals in the tournament, two in the opening game against Tunisia, and then given a standing ovation by the nearly 60,000 attendance when he left the field.

In March 2004, he was named one of the top 125 living footballers by Pelé.

In 2006, he was stripped of the captaincy – something he said he had seen coming, as there had been a change in attitude from some staff members. This had probably been due to his proposed move to the Middle East, which had been growing in speculation. At the end of the season, he refused a one-year extension in order to move to Qatar.

After just one season in Qatar, Football League Championship side Hull City signed Okocha on a free transfer in 2007, after the player had been linked to Real Salt Lake and Sydney FC. It was a move he made saying that “God had told him to do so”. He however was not able to contribute greatly to Hull’s promotion campaign due to fitness and constant injury problems, playing only 18 games and scoring no goals. Hull still succeeded in winning promotion to the Premier League, for the first time in their 104-year history. At the end of the season, after changing his mind on a proposed retirement due to Hull’s promotion, he was released by the club, which ultimately sent him into retirement.

Okocha joined Bolton Wanderers on a free transfer after leaving PSG in the summer of 2002 after the FIFA World Cup. His debut season, despite being hampered by injuries, made him a favourite with the Bolton fans, with the team printing shirts with the inscription “Jay-Jay – so good they named him twice”. He steered the team away from relegation with seven goals, including the team Goal of the Season in the vital league win against West Ham United. This was voted Bolton’s best Premier League goal in a fans vote in 2008. The next season saw Okocha receive more responsibility as he was given the captain’s armband following Guðni Bergsson’s retirement. As captain he led Bolton to their first cup final in nine years where they finished runners-up in the 2004 Football League Cup to Middlesbrough.

Following Bolton’s relegation from the Premier League in 2012, Okocha stated that his time at the club was now rendered a waste of time, because the club had not invested and improved on the foundations that were laid during his time there.

On 21 February 2015, Okocha was elected as the Chairman of the Delta State Football Association.

In April 2015, Okocha expressed his interest in becoming the Nigeria Football Federation president; and he is vigorously pursuing it.

In June 2019, it was reported that Okocha had been charged with alleged money laundering in Scotland.