St. John's County Homes With Guest Suite

Are you a home buyer who could use the extra living space a guest suite provides? Featured here are all St. John's County homes for sale with a guest suite. If you’re interested in any of the St. John's County guest suite home listings that you see below, just click the "Ask a Question" button when viewing the details of that property. Our St. John's County real estate agents can provide you with disclosures, past sales history, dates and prices of properties recently sold nearby, and other details related to St. John's County homes with a guest suite.

And if you'd like to stay up-to-date on St. John's County homes with a guest suite, we also invite you to register for a free account so that you can receive email alerts whenever new listings hit the market that fit your search criteria, allowing you to stay one-step ahead of other buyers in the area. And remember to call or text us directly with any additional questions you have about buying or selling a home in St. John's County, Florida. 

Search St. John's County Homes With Guest Suite

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New
598 East Kesley Ln, St Johns

$1,800,000

598 East Kesley Ln, St Johns

6 Beds 6 Baths 5,955 SqFt Single Family Residence MLS® # 1174043
488 East Kesley Ln, St Johns

$1,675,000

↓ $50,000

488 East Kesley Ln, St Johns

5 Beds 5 Baths 5,635 SqFt Single Family Residence MLS® # 1170624
300 St Johns Forest Blvd, St Johns

$1,250,000

300 St Johns Forest Blvd, St Johns

6 Beds 5 Baths 4,814 SqFt Single Family Residence MLS® # 1174183
New
175 Marquesa Cir, St Johns

$983,547

175 Marquesa Cir, St Johns

5 Beds 5 Baths 3,459 SqFt Single Family Residence MLS® # 1176828
358 Pine Haven Dr, St Johns

$970,000

358 Pine Haven Dr, St Johns

4 Beds 4 Baths 3,498 SqFt Single Family Residence MLS® # 1175642
113 Marquesa Cir, St Johns

$925,000

113 Marquesa Cir, St Johns

4 Beds 3 Baths 2,607 SqFt Single Family Residence MLS® # 1172699
New
143 Pine Haven Dr, St Johns

$919,000

143 Pine Haven Dr, St Johns

3 Beds 3 Baths 2,671 SqFt Single Family Residence MLS® # 1176271
1224 Creek Bend Rd, St Johns

$789,000

1224 Creek Bend Rd, St Johns

4 Beds 4 Baths 3,092 SqFt Single Family Residence MLS® # 1175385
119 Rockcreek Dr, St Johns

$789,000

119 Rockcreek Dr, St Johns

5 Beds 4 Baths 3,512 SqFt Single Family Residence MLS® # 1168794
23 Silkgrass Pl, St Johns

$731,033

↓ $10,000

23 Silkgrass Pl, St Johns

6 Beds 5 Baths 2,800 SqFt Single Family Residence MLS® # 1163749
400 Heritage Oaks Dr, St Johns

$679,000

↓ $21,000

400 Heritage Oaks Dr, St Johns

5 Beds 4 Baths 3,325 SqFt Single Family Residence MLS® # 1164434
700 Rum Runner Way, St Johns

$630,990

700 Rum Runner Way, St Johns

4 Beds 3 Baths 2,515 SqFt Duplex MLS® # 1173952
405 North Buck Board Dr, St Johns

$625,000

↓ $25,000

405 North Buck Board Dr, St Johns

4 Beds 3 Baths 2,678 SqFt Single Family Residence MLS® # 1175575
1092 Durbin Parke Dr, St Johns

$625,000

1092 Durbin Parke Dr, St Johns

4 Beds 2 Baths 2,810 SqFt Single Family Residence MLS® # 1175794
121 Tollerton Ave, St Johns

$580,000

121 Tollerton Ave, St Johns

5 Beds 3 Baths 2,849 SqFt Single Family Residence MLS® # 1175995
618 Rum Runner Way, St Johns

$579,990

↓ $20,000

618 Rum Runner Way, St Johns

4 Beds 3 Baths 2,054 SqFt Duplex MLS® # 1131822
630 Rum Runner Way, St Johns

$579,990

↓ $20,000

630 Rum Runner Way, St Johns

4 Beds 3 Baths 2,054 SqFt Duplex MLS® # 1131846
635 Rum Runner Way, St Johns

$579,990

↓ $20,000

635 Rum Runner Way, St Johns

4 Beds 3 Baths 2,054 SqFt Duplex MLS® # 1131847
643 Rum Runner Way, St Johns

$579,990

↓ $20,000

643 Rum Runner Way, St Johns

4 Beds 3 Baths 2,054 SqFt Duplex MLS® # 1131849
177 Pinellas Way, St Johns

$514,250

↑ $528

177 Pinellas Way, St Johns

2 Beds 2 Baths 1,686 SqFt Single Family Residence MLS® # 1152207