Whelehan made his senior debut for Offaly in a Leinster championship game against Meath in 1998. He played no part in Offaly's subsequent provincial final defeat by Kilkenny. This defeat prompted the Offaly manager, Babs Keating, to describe the team as "sheep in a heap", and he promptly resigned. It looked as if Offaly's championship hopes were in disarray, however, they overcame Antrim in the All-Ireland quarter-final and qualified to meet Clare in the semi-final. The first game ended in a draw and had to be replayed, however, the replay was ended early because of a time-keeping error by the referee Jimmy Cooney. Following a protest on the pitch of Croke Park by the Offaly supporters it was decided that Clare and Offaly would meet for a third time. Whelehan's side won the third game and qualified to play Kilkenny in the final. On that day Brian Whelehan delivered one of his greatest-ever Offaly performances, scoring 1-6. Offaly reversed the Leinster final defeat by winning the All-Ireland final by 2-13 to 1-16. It was Whelehan's first All-Ireland medal.
Offaly surrendered their All-Ireland crown the following year but returned to the All-Ireland decider again in 2000 in a repeat of the Leinster final. Kilkenny's D.J. Carey capitalised on an Offaly mistake after just six minutes to start a goal-fest for "the Cats". Carey scored 2–4 in all, sharing his second goal with Henry Shefflin who also scored a goal in the second-half. At the full-time whistle Kilkenny were the champions by 5–15 to 1–14.
The following few seasons proved difficult as Kilkenny went on to dominate the provincial championship. Whelehan decided to retire from inter-county hurling after the 2004 championship.