Tilkowski debuted for the West German national team in 1957. He was expected to be the first-choice keeper for the 1962 FIFA World Cup in Chile, but was demoted by coach Sepp Herberger the day before the opening match. Tilkowski destroyed his hotel room in anger and did not play for the national team for two years, but was eventually called up again. Under Herberger's successor Helmut Schön, Tilkowski was the first-choice in goal for the 1966 FIFA World Cup in England. The team would lose the final 4–2 to the hosts. The final was remembered as English forward Geoff Hurst scored his controversial second goal en route to a hat-trick. In the 101st minute, 11 minutes into the extra time, Hurst's shot hit the crossbar, the ball then bounced on the ground before being cleared by defender Wolfgang Weber. The goal was given by referee Gottfried Dienst after consultation with linesman Tofiq Bahramov, giving England a 3–2 lead. Photographic evidence would later show that the ball did not cross the line. Unlike most of his team-mates, Tilkowski never resigned himself to the decision, pointing out whenever he could that it was flawed – though with a sense of humour. In 2009 he agreed to unveil a statue in Azerbaijan of Tofiq Bahramov, the linesman who had indicated that the goal should stand. He played for West Germany another year, before being superseded in the national team by Sepp Maier.