diff --git a/fluffy/conf.nim b/fluffy/conf.nim
index 424c18d4e..b165b3f2c 100644
--- a/fluffy/conf.nim
+++ b/fluffy/conf.nim
@@ -302,6 +302,22 @@ type
       name: "force-prune"
     .}: bool
 
+    contentCacheSize* {.
+      hidden,
+      desc:
+        "Size of the in memory local content cache. This is the max number " &
+        "of content values that can be stored in the cache.",
+      defaultValue: defaultPortalProtocolConfig.contentCacheSize,
+      name: "content-cache-size"
+    .}: int
+
+    disableContentCache* {.
+      hidden,
+      desc: "Disable the in memory local content cache",
+      defaultValue: defaultPortalProtocolConfig.disableContentCache,
+      name: "disable-content-cache"
+    .}: bool
+
     disablePoke* {.
       hidden,
       desc: "Disable POKE functionality for gossip mechanisms testing",
diff --git a/fluffy/fluffy.nim b/fluffy/fluffy.nim
index 3073cb585..b3084b85d 100644
--- a/fluffy/fluffy.nim
+++ b/fluffy/fluffy.nim
@@ -182,7 +182,8 @@ proc run(
   let
     portalProtocolConfig = PortalProtocolConfig.init(
       config.tableIpLimit, config.bucketIpLimit, config.bitsPerHop, config.radiusConfig,
-      config.disablePoke, config.maxGossipNodes,
+      config.disablePoke, config.maxGossipNodes, config.contentCacheSize,
+      config.disableContentCache,
     )
 
     portalNodeConfig = PortalNodeConfig(
diff --git a/fluffy/network/state/state_network.nim b/fluffy/network/state/state_network.nim
index 1c5f25cce..56a2ddad1 100644
--- a/fluffy/network/state/state_network.nim
+++ b/fluffy/network/state/state_network.nim
@@ -79,16 +79,15 @@ proc getContent(
   let
     contentKeyBytes = key.toContentKey().encode()
     contentId = contentKeyBytes.toContentId()
+    maybeLocalContent = n.portalProtocol.getLocalContent(contentKeyBytes, contentId)
 
-  if n.portalProtocol.inRange(contentId):
-    let contentFromDB = n.contentDB.get(contentId)
-    if contentFromDB.isSome():
-      let contentValue = V.decode(contentFromDB.get()).valueOr:
-        error "Unable to decode state content value from database"
-        return Opt.none(V)
+  if maybeLocalContent.isSome():
+    let contentValue = V.decode(maybeLocalContent.get()).valueOr:
+      error "Unable to decode state local content value"
+      return Opt.none(V)
 
-      info "Fetched state content value from database"
-      return Opt.some(contentValue)
+    info "Fetched state local content value"
+    return Opt.some(contentValue)
 
   let
     contentLookupResult = (
@@ -106,7 +105,9 @@ proc getContent(
     warn "Validation of retrieved state content failed"
     return Opt.none(V)
 
-  n.portalProtocol.storeContent(contentKeyBytes, contentId, contentValueBytes)
+  n.portalProtocol.storeContent(
+    contentKeyBytes, contentId, contentValueBytes, cacheContent = true
+  )
 
   Opt.some(contentValue)
 
diff --git a/fluffy/network/wire/portal_protocol.nim b/fluffy/network/wire/portal_protocol.nim
index bf4af975e..c2ce49cd2 100644
--- a/fluffy/network/wire/portal_protocol.nim
+++ b/fluffy/network/wire/portal_protocol.nim
@@ -74,6 +74,12 @@ declareCounter portal_gossip_with_lookup,
 declareCounter portal_gossip_without_lookup,
   "Portal wire protocol neighborhood gossip that did not require a node lookup",
   labels = ["protocol_id"]
+declareCounter portal_content_cache_hits,
+  "Portal wire protocol local content lookups that hit the cache",
+  labels = ["protocol_id"]
+declareCounter portal_content_cache_misses,
+  "Portal wire protocol local content lookups that don't hit the cache",
+  labels = ["protocol_id"]
 
 declareCounter portal_poke_offers,
   "Portal wire protocol offers through poke mechanism", labels = ["protocol_id"]
@@ -151,6 +157,8 @@ type
 
   RadiusCache* = LRUCache[NodeId, UInt256]
 
+  ContentCache = LRUCache[ContentId, seq[byte]]
+
   ContentKV* = object
     contentKey*: ContentKeyByteList
     content*: seq[byte]
@@ -172,6 +180,7 @@ type
     routingTable*: RoutingTable
     baseProtocol*: protocol.Protocol
     toContentId*: ToContentIdHandler
+    contentCache: ContentCache
     dbGet*: DbGetHandler
     dbPut*: DbStoreHandler
     dataRadius*: DbRadiusHandler
@@ -186,6 +195,7 @@ type
     disablePoke: bool
     pingTimings: Table[NodeId, chronos.Moment]
     maxGossipNodes: int
+    config*: PortalProtocolConfig
 
   PortalResult*[T] = Result[T, string]
 
@@ -568,6 +578,8 @@ proc new*(
     ),
     baseProtocol: baseProtocol,
     toContentId: toContentId,
+    contentCache:
+      ContentCache.init(if config.disableContentCache: 0 else: config.contentCacheSize),
     dbGet: dbGet,
     dbPut: dbPut,
     dataRadius: dbRadius,
@@ -578,6 +590,7 @@ proc new*(
     disablePoke: config.disablePoke,
     pingTimings: Table[NodeId, chronos.Moment](),
     maxGossipNodes: config.maxGossipNodes,
+    config: config,
   )
 
   proto.baseProtocol.registerTalkProtocol(@(proto.protocolId), proto).expect(
@@ -1590,7 +1603,12 @@ proc storeContent*(
     contentKey: ContentKeyByteList,
     contentId: ContentId,
     content: seq[byte],
+    cacheContent = false,
 ): bool {.discardable.} =
+  if cacheContent and not p.config.disableContentCache:
+    # We cache content regardless of whether it is in our radius or not
+    p.contentCache.put(contentId, content)
+
   # Always re-check that the key is still in the node range to make sure only
   # content in range is stored.
   if p.inRange(contentId):
@@ -1600,6 +1618,25 @@ proc storeContent*(
   else:
     false
 
+proc getLocalContent*(
+    p: PortalProtocol, contentKey: ContentKeyByteList, contentId: ContentId
+): Opt[seq[byte]] =
+  # The cache can contain content that is not in our radius
+  let maybeContent = p.contentCache.get(contentId)
+  if maybeContent.isSome():
+    portal_content_cache_hits.inc(labelValues = [$p.protocolId])
+    return maybeContent
+
+  portal_content_cache_misses.inc(labelValues = [$p.protocolId])
+
+  # Check first if content is in range, as this is a cheaper operation
+  # than the database lookup.
+  if p.inRange(contentId):
+    doAssert(p.dbGet != nil)
+    p.dbGet(contentKey, contentId)
+  else:
+    Opt.none(seq[byte])
+
 proc seedTable*(p: PortalProtocol) =
   ## Seed the table with specifically provided Portal bootstrap nodes. These are
   ## nodes that must support the wire protocol for the specific content network.
diff --git a/fluffy/network/wire/portal_protocol_config.nim b/fluffy/network/wire/portal_protocol_config.nim
index e6081fbbd..da70a636f 100644
--- a/fluffy/network/wire/portal_protocol_config.nim
+++ b/fluffy/network/wire/portal_protocol_config.nim
@@ -41,12 +41,16 @@ type
     radiusConfig*: RadiusConfig
     disablePoke*: bool
     maxGossipNodes*: int
+    contentCacheSize*: int
+    disableContentCache*: bool
 
 const
   defaultRadiusConfig* = RadiusConfig(kind: Dynamic)
   defaultRadiusConfigDesc* = $defaultRadiusConfig.kind
   defaultDisablePoke* = false
-  defaultMaxGossipNodes = 4
+  defaultMaxGossipNodes* = 4
+  defaultContentCacheSize* = 100
+  defaultDisableContentCache* = false
   revalidationTimeout* = chronos.seconds(30)
 
   defaultPortalProtocolConfig* = PortalProtocolConfig(
@@ -55,6 +59,8 @@ const
     radiusConfig: defaultRadiusConfig,
     disablePoke: defaultDisablePoke,
     maxGossipNodes: defaultMaxGossipNodes,
+    contentCacheSize: defaultContentCacheSize,
+    disableContentCache: defaultDisableContentCache,
   )
 
 proc init*(
@@ -65,6 +71,8 @@ proc init*(
     radiusConfig: RadiusConfig,
     disablePoke: bool,
     maxGossipNodes: int,
+    contentCacheSize: int,
+    disableContentCache: bool,
 ): T =
   PortalProtocolConfig(
     tableIpLimits:
@@ -73,6 +81,8 @@ proc init*(
     radiusConfig: radiusConfig,
     disablePoke: disablePoke,
     maxGossipNodes: maxGossipNodes,
+    contentCacheSize: contentCacheSize,
+    disableContentCache: disableContentCache,
   )
 
 func fromLogRadius*(T: type UInt256, logRadius: uint16): T =
diff --git a/fluffy/rpc/rpc_portal_state_api.nim b/fluffy/rpc/rpc_portal_state_api.nim
index a1d163ddb..c35ae0d27 100644
--- a/fluffy/rpc/rpc_portal_state_api.nim
+++ b/fluffy/rpc/rpc_portal_state_api.nim
@@ -88,7 +88,7 @@ proc installPortalStateApiHandlers*(rpcServer: RpcServer, p: PortalProtocol) =
       keyBytes = ContentKeyByteList.init(hexToSeqByte(contentKey))
       (key, contentId) = validateGetContentKey(keyBytes).valueOr:
         raise invalidKeyErr()
-      maybeContent = p.dbGet(keyBytes, contentId)
+      maybeContent = p.getLocalContent(keyBytes, contentId)
     if maybeContent.isSome():
       return ContentInfo(content: maybeContent.get().to0xHex(), utpTransfer: false)
 
@@ -99,7 +99,7 @@ proc installPortalStateApiHandlers*(rpcServer: RpcServer, p: PortalProtocol) =
 
     validateRetrieval(key, contentValue).isOkOr:
       raise invalidValueErr()
-    p.storeContent(keyBytes, contentId, contentValue)
+    p.storeContent(keyBytes, contentId, contentValue, cacheContent = true)
 
     ContentInfo(content: contentValue.to0xHex(), utpTransfer: foundContent.utpTransfer)
 
@@ -110,7 +110,7 @@ proc installPortalStateApiHandlers*(rpcServer: RpcServer, p: PortalProtocol) =
       keyBytes = ContentKeyByteList.init(hexToSeqByte(contentKey))
       (key, contentId) = validateGetContentKey(keyBytes).valueOr:
         raise invalidKeyErr()
-      maybeContent = p.dbGet(keyBytes, contentId)
+      maybeContent = p.getLocalContent(keyBytes, contentId)
     if maybeContent.isSome():
       return TraceContentLookupResult(content: maybeContent, utpTransfer: false)
 
@@ -124,7 +124,7 @@ proc installPortalStateApiHandlers*(rpcServer: RpcServer, p: PortalProtocol) =
 
     validateRetrieval(key, contentValue).isOkOr:
       raise invalidValueErr()
-    p.storeContent(keyBytes, contentId, contentValue)
+    p.storeContent(keyBytes, contentId, contentValue, cacheContent = true)
 
     res
 
@@ -145,7 +145,7 @@ proc installPortalStateApiHandlers*(rpcServer: RpcServer, p: PortalProtocol) =
       (_, contentId) = validateGetContentKey(keyBytes).valueOr:
         raise invalidKeyErr()
 
-      contentResult = p.dbGet(keyBytes, contentId).valueOr:
+      contentResult = p.getLocalContent(keyBytes, contentId).valueOr:
         raise contentNotFoundErr()
 
     contentResult.to0xHex()
diff --git a/fluffy/tests/wire_protocol_tests/test_portal_wire_protocol.nim b/fluffy/tests/wire_protocol_tests/test_portal_wire_protocol.nim
index 7a7ba7177..11d7b3c72 100644
--- a/fluffy/tests/wire_protocol_tests/test_portal_wire_protocol.nim
+++ b/fluffy/tests/wire_protocol_tests/test_portal_wire_protocol.nim
@@ -375,3 +375,73 @@ procSuite "Portal Wire Protocol Tests":
 
     await proto1.stop()
     await node1.closeWait()
+
+  asyncTest "Local content - Cache enabled":
+    let (proto1, proto2) = defaultTestSetup(rng)
+
+    # proto1 has no radius so the content won't be stored in the local db
+    proto1.dataRadius = proc(): UInt256 =
+      0.u256
+
+    let
+      contentKey = ContentKeyByteList(@[byte 0x01, 0x02, 0x03])
+      contentId = contentKey.toContentId().get()
+      content = @[byte 0x04, 0x05, 0x06]
+
+    check:
+      proto1.storeContent(contentKey, contentId, content) == false
+      proto2.storeContent(contentKey, contentId, content) == true
+
+      proto1.getLocalContent(contentKey, contentId).isNone()
+      proto2.getLocalContent(contentKey, contentId).get() == content
+
+      proto1.storeContent(contentKey, contentId, content, cacheContent = false) == false
+      proto2.storeContent(contentKey, contentId, content, cacheContent = false) == true
+
+      proto1.getLocalContent(contentKey, contentId).isNone()
+      proto2.getLocalContent(contentKey, contentId).get() == content
+
+      proto1.storeContent(contentKey, contentId, content, cacheContent = true) == false
+      proto2.storeContent(contentKey, contentId, content, cacheContent = true) == true
+
+      proto1.getLocalContent(contentKey, contentId).get() == content
+      proto2.getLocalContent(contentKey, contentId).get() == content
+
+    await proto1.stopPortalProtocol()
+    await proto2.stopPortalProtocol()
+
+  asyncTest "Local content - Cache disabled":
+    let (proto1, proto2) = defaultTestSetup(rng)
+    proto1.config.disableContentCache = true
+    proto2.config.disableContentCache = true
+
+    # proto1 has no radius so the content won't be stored in the local db
+    proto1.dataRadius = proc(): UInt256 =
+      0.u256
+
+    let
+      contentKey = ContentKeyByteList(@[byte 0x01, 0x02, 0x03])
+      contentId = contentKey.toContentId().get()
+      content = @[byte 0x04, 0x05, 0x06]
+
+    check:
+      proto1.storeContent(contentKey, contentId, content) == false
+      proto2.storeContent(contentKey, contentId, content) == true
+
+      proto1.getLocalContent(contentKey, contentId).isNone()
+      proto2.getLocalContent(contentKey, contentId).get() == content
+
+      proto1.storeContent(contentKey, contentId, content, cacheContent = false) == false
+      proto2.storeContent(contentKey, contentId, content, cacheContent = false) == true
+
+      proto1.getLocalContent(contentKey, contentId).isNone()
+      proto2.getLocalContent(contentKey, contentId).get() == content
+
+      proto1.storeContent(contentKey, contentId, content, cacheContent = true) == false
+      proto2.storeContent(contentKey, contentId, content, cacheContent = true) == true
+
+      proto1.getLocalContent(contentKey, contentId).isNone()
+      proto2.getLocalContent(contentKey, contentId).get() == content
+
+    await proto1.stopPortalProtocol()
+    await proto2.stopPortalProtocol()