Spurs, with the help of a double from Harry Kane, secured qualification for UEFA's new third-tier club competition with a 3-0 win over Pacos de Ferreira on Thursday.
The presence of Kane, who will be staying at Tottenham despite Manchester City's long-standing interest, is sure to make Spurs one of the favourites to win the tournament.
Nuno Espirito Santo's side were placed into Group G, and have avoided too many arduous journeys, with a trip to Slovenia to face Mura – a team only formed in 2012 – the longest trip in store.
Roma, coached by former Tottenham boss Jose Mourinho, are the tournament's other favorites. The Serie A club will face Zorya Luhansk, CSKA Sofia and Bodo/Glimt in Group C.
The Europa League group stage has been trimmed to 32 teams, with Napoli arguably the headline act.
FA Cup winners Leicester City have been drawn in Group E alongside the Italian giants, as well as Spartak Moscow and Legia Warsaw.
The Premier League's other representatives – West Ham – were drawn in Group H, in which they will face Dinamo Zagreb, Genk and Rapid Vienna.
Steven Gerrard's Rangers were placed into Group A with Lyon, Sparta Prague and Brondby, while Scottish rivals Celtic are in a difficult-looking Group G which includes Bayer Leverkusen, Real Betis and Ferencvaros.
Group E pits Lazio, Marseille, Galatasaray and Lokomotiv Moscow up against each other in what promises to be a thriller, while Monaco, PSV, Real Sociedad and Sturm Graz will battle it out for progression from Group B.
The first matches will take place on September 16, with the group stage of both competitions concluding on December 9.
Europa League group stage draw in full:
Group A: Lyon, Rangers, Sparta Prague, Brondby
Group B: Monaco, PSV Eindhoven, Real Sociedad, Sturm Graz
Group C: Napoli, Leicester City, Spartak Moscow, Legia Warsaw
Group D: Olympiacos, Eintracht Frankfurt, Fenerbahce, Royal Antwerp
Group E: Lazio, Lokomotiv Moscow, Marseille, Galatasaray
Group F: Braga, Red Star Belgrade, Ludogorets, Midtjylland
Group G: Bayer Leverkusen, Celtic, Real Betis, Ferencvaros
Group H: Dinamo Zagreb, Genk, West Ham, Rapid Vienna
Europa Conference League group stage draw in full:
Group A: LASK, Maccabi Tel-Aviv, Alashkert, HJK Helsinki
Group B: Gent, FK Partizan, Flora, Anorthosis
Group C: Roma, Zorya Luhansk, CSKA Sofia, Bodo/Glimt
Group D: AZ Alkmaar, CFR Cluj, Jablonec, Randers
Group E: Slavia Prague, Feyenoord, Union Berlin,
Group F: Copenhagen, PAOK, Slovan Bratislava, Lincoln Red Imps
Group G: Tottenham, Rennes, Vitesse, Mura
Group H: Basel, Qarabag, Kairat, Omonoia