Recruited from the Ascot ValeFootball Club, Towner made his debut for Essendon Firsts as a reserve in the second home-and-away round match against South Melbourne at the Lake Oval on 2 May 1953. In his first year, he played 11 senior matches, including the Firsts Semi-Final team that lost 5.11 to Footscray's 6.13. He played 16 senior games in 1954, a single game in 1955, 10 games in 1956, 16 games in 1957 — he played on the half-back flank in the losing Essendon Grand Final team of 1957 — 16 games in 1958, and 17 games in 1959. His game at full-back for the Essendon 1959 Grand Final team, which was beaten by Melbourne 17.13 to 11.12, was his last game for Essendon. Well-liked at Essendon, he left Essendon due to an employment transfer to Western Australia. He played at full-back with West Perth for three years. He later moved to Queensland and was captain-coach of Surfers Paradise Football Club in 1965.
In 1953 and 1954 Towner played on the forward line. With a lot of pace across the ground, and strong in the air, he was tried at full-forward as a replacement for the injured John Coleman in 1954; however, once at full-forward, he demonstrated that he was not a very accurate kick. Once he was switched to defence, he was highly successful, initially on the half-back flank and, later in his career at Essendon, as the team's regular full-back. As a full-back, much of his game was centred on his ability to judge and understand the manner in which his full-forward opponent went for the ball; and much of his value to Essendon was his ability to consistently punch the ball out of the hands of a full-forward attempting to mark over his head. In particular, he always had "the wood" over South Melbourne's Brownlow Medallist Fred Goldsmith, holding him goal-less on several occasions; and it was enthralling as a spectator, to see the tussle between the two — in particular, to see the highly skilled full-back-turned-full-forward Goldsmith getting more and more frustrated each time that the fist of the highly skilled full-forward-turned-full-back Towner came between his own outstretched hands and, yet again, punched the ball 20 metres towards the Essendon goals.