Venison had originally made his debut for the Black Cats, aged just 17, on 10 October 1981 in the 2–0 league defeat to Notts County at Meadow Lane. He went on to play in 20 league games that season scoring one goal in the process. The steady and reliable right full-back settled into first team football well at Roker Park and became a firm favourite in 1983–84, when he missed just one league game.
Venison had been selected to represent England at under-21 level on 10 occasions from 1982 until 1986.
At the end of the 1984–85 season, the same season in which they had reached the League Cup final, Sunderland were relegated to the Second Division. After Sunderland's failure to win promotion in 1985–86, Venison asked for a transfer as his Sunderland contract neared expiry in 1986, so he wrote to every club in English football's top division to ask if they were interested in him.
By the end of the 1985–86 season he had made a total of 205 appearances for the Wearsiders; 173 of them in the Football League. He had managed two goals.
Venison made his Liverpool debut on 16 August 1986 in the traditional curtain raiser at Wembley, the Charity Shield, Liverpool faced derby rivals Everton, who had lost out to the Reds in both the previous season's League and FA Cup campaigns. The usual high tempo game ended in a 1–1 draw with both clubs sharing the shield. He featured in 33 out of 42 league games that season.
Venison was a League Cup final loser again in his first season at Anfield, when Liverpool were defeated by Arsenal in the 1987 final. He was also denied the chance of league title glory as the Reds were beaten into second place in the league by their neighbours Everton.
The next season would see Venison's first goal for the club, it came on 29 August 1988 in the 4–1 thrashing of Nottingham Forest in the quarter finals of the Centenary trophy. Venison featured in more games but with fewer starts, often named as one of the two permitted substitutes.
Venison, along with his teammates, rallied round the bereaved families of the Hillsborough disaster in April 1989, attending a number of the funerals, he then played his role as Liverpool reached the final of the FA Cup again. Dalglish brought him on as an extra-time substitute as Liverpool defeated Merseyside rivals Everton 3–2. They later lost the League title in a decider against Arsenal at Anfield after Michael Thomas scored the winner with virtually the last kick of the whole season. Venison was on the bench again.
1990 saw Venison play 25 times in the league and earn another championship medal as Liverpool secured their 18th top division title.
Venison made his debut of the Magpies on 15 August 1992 in the 3–2 league win over Southend United at St James' Park, Venison enjoyed a tremendous beginning to his Newcastle career as they won their first eleven league games in a row, leaving them runaway Leaders of Division One and looking uncatchable in the promotion race by October. The run came to an end when they lost to a last minute goal at home against Grimsby Town; they fell just 2 games short of the record 13 straight victories that had been set seven years earlier by Reading in the old Third Division. Keegan got his team to play in an exciting, attacking way with them becoming a talking point within the game for their exuberant style of play along with their mean defence which included a revitalised Venison as well as the likes of John Beresford and Steve Howey. Newcastle went on to become Division One champions, winning the title with a 2–0 away win, coincidentally at Grimsby, thus gaining promotion to the Premier League.
Venison remained a crucial part of the Newcastle defence as they returned to the top FLIGHT in 1993–94, and helped them hit the ground running as they secured a third-place finish (though they never really looked like catching up with the leading pair that consisted of champions Manchester United and runners-up Blackburn Rovers. This gave the Magpies a place in Europe (the UEFA Cup) for the first time since the 1970s.
In 1994, aged 30, Venison was picked to represent his country by new coach Terry Venables. The call-up came as a surprise, not least to Venison, but he played well in both of his full international appearances. His debut came on 7 September 1994 in the 2–0 friendly victory over the United States; his only other appearance for his country came on 29 March 1995 in a 0–0 friendly draw with Uruguay. Both games were played at Wembley.
Venison spent just under 5 months with the Turkish side, playing eight games, before he was on the move once more. He joined Southampton for £850,000 on 25 October 1995. He played 27 Premier League games that season as Southampton avoided relegation on goal difference and reached the FA Cup quarter finals.
He played two more games for the Saints in the 1996–97 season (by which time Souness was manager of Southampton, the third club Venison had played under him at), before he suffered a back injury which led to him announcing his retirement for playing on 20 October 1996 at the age of 32.
After retirement, Venison took up punditry; firstly for Sky Sports, and then, from 1997 to 2002, for ITV.
In the early 2000s, Venison launched an on-line Sports memorabilia auction site. The company "bid4sport.com" was a not-for-profit company and raised money for charities. Julie Venison was also involved in Bid4sport providing Business support and book-keeping for the venture. The company was initially based on the outskirts of Romsey before expanding and moving to premises to the west of Fareham. The venture was created with the help of friend and co-professional Brad Friedel. Venison sold Bid4sport shortly before his family relocated to the United States.
Venison also made an appearance as himself in the 2001 comedy film, Mike Bassett: England Manager.
Venison moved to the United States in 2003, firstly to Laguna Beach, and then Los Angeles. He worked in property development for a short time, before his friend Oliver Wyss, convinced him to return to football. Venison became Technical Director of Orange County Blues, before succeeding Wyss as head coach to see out the 2016 USL Pro season.
The following campaign was a non-event for Venison as he only managed a total of 14 appearances in all competitions, however, this did include another Wembley appearance as the Reds faced bitter rivals Manchester United in the Charity Shield, again, the Reds had to share the trophy as they drew 1–1 with their North West rivals.
In 2016, he was given his first head coaching role at Orange County Blues, succeeding Oliver Wyss.