The Chicago Blackhawks initially owned his rights although he never cracked their lineup. Instead he toiled in their minor-league system first, for the most part with the St. Louis Braves, where he shared honours with Garry Peters as the league's Rookie of the Year. Then in 1964-65, he stepped up to the Buffalo Bisons of the AHL for one year before being claimed by the Boston Bruins in an intra-league draft in 1965.

As a journeyman defenseman though, it was difficult for Popiel to catch on with an original-six lineup. So it was back to the minors after only three Bruin games, this time with the Hershey Bears of the AHL. In 1967, as the NHL expanded, the Los Angeles Kings who tucked him away with their AHL affiliate, the Springfield Kings, claimed Popiel. But the following year he was traded to the Detroit Red Wings where he finally got his first full season in the NHL before splitting 1969-70 between the Wings and their minor-league affiliate in Cleveland.

In 1970-71, the Vancouver Canucks who used the veteran to stabilize their newly formed blueline corps again claimed Popiel in an Expansion Draft, this time. But as was always the case in the NHL, he tended to be used as a defensive stopgap who was useful only so long as there were injuries or short-term holes to be filled on the roster.

Not long after the start of the 1971-72 season, Popiel was dispatched to the Rochester Americans where he stayed only long enough to work out a deal with the Houston Aeros of the newly formed World Hockey Association. In Houston, he finally found a stable home as a blueline regular for six seasons. But by 1978, he felt he'd had his fill of the WHA. So he was quick to jump at an offer to play for Innsbruck in Austria for one season.

The following year, Edmonton Oilers' GM Glenn Sather brought Popiel back to the NHL as a fill-in during a rash of injuries. He savoured every moment of his ten games with the Oilers before rounding out his lengthy pro career with the Houston Apollos and the Muskegon Mohawks, retiring in 1981.