Huckerby was promoted to the first team at Sincil Bank by Keith Alexander, but also played under the stewardship of both Sam Ellis and Steve Wicks before being sold in 1995.

Huckerby made a three division step up by signing for Premier League title contenders Newcastle United in a £400,000 deal in 1995.

The striker's pace and dribbling ability, combined with a very successful partnership with Dion Dublin saw Huckerby play a key role at Coventry.

Huckerby played a major role in Coventry's Premier League survival, culminating with a final day 2–1 win at Tottenham Hotspur in 1997.

His success with the Sky Blues continued throughout the following season as Coventry enjoyed a ten-game unbeaten run and reached the quarter finals of the FA Cup, narrowly losing on penalties to Sheffield United.

[6] He had to compete for a place in the team with some players such as Mark Viduka, Alan Smith and Michael Bridges and as a result he was never a regular, although he did score against Partizan Belgrade in the 1999–2000 UEFA Cup,[7] and in a 6–0 win against Beşiktaş in the 2000–01 Champions League.

[9] Although the club did eventually go down, he stayed on and won a First Division championship medal, adding 26 goals in all competitions during the campaign, including two hat-tricks.

Huckerby started the new campaign as first choice, and scored the team's first goal of the season, a header against former employer Newcastle that secured a 1–0 win.

Huckerby spent a three-month loan spell with Norwich City, before signing permanently in December 2003, for a fee of £750,000, which rose to £1 million when the Canaries were promoted at the end of the season.

[16] In 2012, Huckerby returned to Carrow Road to play in Adam Drury's testimonial match against Celtic, coming on in the 76th minute showing his trademark bursts of pace and skill.

Former Celtic and Norwich striker John Hartson who was co-commentating on Setanta Sports claimed he looked fit and sharp enough still to be playing professionally.

[17] Huckerby moved to the United States joining Major League Soccer club, San Jose Earthquakes in July 2008.

On 30 August, he headed in the winning goal in the side's 2–1 victory over Kansas City Wizards, extending San Jose's unbeaten streak to seven games.