Whatmough was born in Gosport, and played for Southampton before moving to Portsmouth Academy in 2009, aged 13. He signed a two-year scholarship deal with Pompey on 6 July 2012.
On 14 August 2012, aged only 15, Whatmough appeared on the bench in a 0–3 away defeat against Plymouth Argyle. He finished the season with 26 youth appearances, with the Academy being crowned champions.
On 19 August 2013, Whatmouth signed a three-year professional deal. On 28 September he appeared again on the bench, in a 2–4 away defeat against York City.
On 26 November, Whatmough made his professional debut, starting in a 1–2 home loss against Southend United.
On 16 December, Whatmough was called up to train with England U18's. He then made his debut international debut on 5 March of the following year, starting in a 1–2 loss against Croatia at St George's Park.