He returned to English football in August 2017, when he joined Ipswich Town and later Derby County before signing for Coventry City in July 2021, in January 2023 Waghorn joined Huddersfield Town on loan, before re-joining Derby County in August 2023, before being released by the club in June 2024.

After a spell as a free agent, he signed Northampton Town in November 2024 on short-term deal before leaving in December 2024, in February 2025 Waghorn retired from professional football.

Waghorn scored the first hat-trick of his career on 12 December 2007 in a 6–1 win against Norwich City in the FA Youth Cup third round.

On 6 August 2009, Waghorn joined Leicester City on loan until 11 January 2010, having turned down interest from Carlisle United.

[20] On 31 August 2010, Waghorn rejoined Leicester City on a permanent deal for a fee rising to £3 million to help fund Sunderland's record signing Asamoah Gyan.

[21] He was disappointed with the lack of opportunities at his former club,[22] and happily dropped down a division because the lure of playing regular football was too good to turn down.

[26] Nonetheless, injury concerns at the club prevented Waghorn from joining Derby County on loan during the January 2011 transfer window.

[30] On 27 September 2011 against Doncaster Rovers at the Keepmoat Stadium, Matty Fryatt found himself with space to deliver a low cross along the six-yard box and although Neil Sullivan might have been disappointed not to cut it out, Waghorn was there to apply the finish from close range.

[32] After making only two substitute appearances for Leicester, Waghorn joined Millwall on a three-month loan deal on 12 September 2013.

[39] On 20 July 2015, Waghorn signed a three-year deal with Scottish Championship side Rangers along with Wigan teammate James Tavernier.

[50] However, it did not affect his goalscoring form, as Waghorn netted five in his first four games with strikes against Motherwell,[51] Annan Athletic[52] and a brace against Stranraer[53] before scoring Rangers first Scottish Premiership goal of the season in a 1–1 draw at home to Hamilton Academical.

[56] Upon his return from injury, Waghorn struggled for goal-scoring form, although he did net the third hat-trick of his Rangers career in a League Cup match against Queen of the South.

On 6 March he netted a brace in a 2–1 away win over Sheffield Wednesday at Hillsborough, including scoring a late free-kick from outside the 18 yard box.

[72] After 404 days, Wagehorn finally netted his second Sky Blues' goal with a vital penalty kick late on in a 1–0 win over Sheffield United.

On 13 January 2023, Waghorn joined fellow EFL Championship side Huddersfield Town for the remainder of the 2022–23 season.

[77] He was set to return in January 2024, but after a setback in his rehab he was ruled out for "foreseeable" by Derby head coach Paul Warne.

[78] Waghorn returned to action on 27 February 2024, against Charlton Athletic[79] and scored his first goal in five months in a 3–0 win at Bristol Rovers on 9 March 2024.

[80] Waghorn made 27 appearances for Derby during the season, scoring seven times as they secured promotion to the Championship after finishing second-place in the League One table.

[89] In his second appearance for the under-21 team, Waghorn was in the starting line-up, scoring a header against Israel from an Alex Oxlade-Chamberlain cross.