diff --git a/matrix_content_scanner/crypto.py b/matrix_content_scanner/crypto.py
new file mode 100644
index 0000000..58f9495
--- /dev/null
+++ b/matrix_content_scanner/crypto.py
@@ -0,0 +1,91 @@
+#  Copyright 2022 The Matrix.org Foundation C.I.C.
+#
+#  Licensed under the Apache License, Version 2.0 (the "License");
+#  you may not use this file except in compliance with the License.
+#  You may obtain a copy of the License at
+#
+#      http://www.apache.org/licenses/LICENSE-2.0
+#
+#  Unless required by applicable law or agreed to in writing, software
+#  distributed under the License is distributed on an "AS IS" BASIS,
+#  WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+#  See the License for the specific language governing permissions and
+#  limitations under the License.
+import json
+import logging
+from typing import TYPE_CHECKING
+
+from olm.pk import PkDecryption, PkDecryptionError, PkMessage
+
+from matrix_content_scanner.utils.constants import ErrCode
+from matrix_content_scanner.utils.errors import ContentScannerRestError
+from matrix_content_scanner.utils.types import JsonDict
+
+if TYPE_CHECKING:
+    from matrix_content_scanner.mcs import MatrixContentScanner
+
+
+logger = logging.getLogger(__name__)
+
+
+class CryptoHandler:
+    """Handler for handling Olm-encrypted request bodies."""
+
+    def __init__(self, mcs: "MatrixContentScanner") -> None:
+        key = mcs.config.crypto.pickle_key
+        path = mcs.config.crypto.pickle_path
+        try:
+            # Try reading the pickle from disk.
+            with open(path, "r") as fp:
+                pickle = fp.read()
+
+            # Create a PkDecryption object with the content and key.
+            self._decryptor: PkDecryption = PkDecryption.from_pickle(
+                pickle=pickle.encode("ascii"),
+                passphrase=key,
+            )
+
+            logger.info("Loaded Olm pickle from %s", path)
+        except FileNotFoundError:
+            # If the pickle file doesn't exist, try creating it.
+            self._decryptor = PkDecryption()
+            pickle_bytes = self._decryptor.pickle(passphrase=key)
+
+            logger.info(
+                "Olm pickle not found, generating one and saving it at %s", path
+            )
+
+            with open(path, "w+") as fp:
+                fp.write(pickle_bytes.decode("ascii"))
+
+        self.public_key = self._decryptor.public_key
+
+    def decrypt_body(self, ciphertext: str, mac: str, ephemeral: str) -> JsonDict:
+        """Decrypts an Olm-encrypted body.
+
+        Args:
+            ciphertext: The encrypted body's ciphertext.
+            mac: The encrypted body's MAC.
+            ephemeral: The encrypted body's ephemeral key.
+
+        Returns:
+            The decrypted body, parsed as JSON.
+        """
+        try:
+            decrypted = self._decryptor.decrypt(
+                message=PkMessage(
+                    ephemeral_key=ephemeral,
+                    mac=mac,
+                    ciphertext=ciphertext,
+                )
+            )
+        except PkDecryptionError as e:
+            logger.error("Failed to decrypt encrypted body: %s", e)
+            raise ContentScannerRestError(
+                http_status=400,
+                reason=ErrCode.FAILED_TO_DECRYPT,
+                info=str(e),
+            )
+
+        # We know that `decrypted` parses as a JsonDict.
+        return json.loads(decrypted)  # type: ignore[no-any-return]
diff --git a/matrix_content_scanner/mcs.py b/matrix_content_scanner/mcs.py
index 57d8333..6934698 100644
--- a/matrix_content_scanner/mcs.py
+++ b/matrix_content_scanner/mcs.py
@@ -24,6 +24,7 @@
 
 from matrix_content_scanner import logutils
 from matrix_content_scanner.config import MatrixContentScannerConfig
+from matrix_content_scanner.crypto import CryptoHandler
 from matrix_content_scanner.httpserver import HTTPServer
 from matrix_content_scanner.scanner.file_downloader import FileDownloader
 from matrix_content_scanner.scanner.scanner import Scanner
@@ -58,6 +59,10 @@ def file_downloader(self) -> FileDownloader:
     def scanner(self) -> Scanner:
         return Scanner(self)
 
+    @cached_property
+    def crypto_handler(self) -> CryptoHandler:
+        return CryptoHandler(self)
+
     def start(self) -> None:
         """Start the HTTP server and start the reactor."""
         setup_logging()
diff --git a/tests/test_crypto.py b/tests/test_crypto.py
new file mode 100644
index 0000000..e5d224f
--- /dev/null
+++ b/tests/test_crypto.py
@@ -0,0 +1,43 @@
+#  Copyright 2022 The Matrix.org Foundation C.I.C.
+#
+#  Licensed under the Apache License, Version 2.0 (the "License");
+#  you may not use this file except in compliance with the License.
+#  You may obtain a copy of the License at
+#
+#      http://www.apache.org/licenses/LICENSE-2.0
+#
+#  Unless required by applicable law or agreed to in writing, software
+#  distributed under the License is distributed on an "AS IS" BASIS,
+#  WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+#  See the License for the specific language governing permissions and
+#  limitations under the License.
+import json
+import unittest
+
+from olm.pk import PkEncryption
+
+from tests.testutils import get_content_scanner
+
+
+class CryptoHandlerTestCase(unittest.TestCase):
+    def setUp(self) -> None:
+        self.crypto_handler = get_content_scanner().crypto_handler
+
+    def test_decrypt(self) -> None:
+        """Tests that an Olm-encrypted payload is successfully decrypted."""
+        payload = {"foo": "bar"}
+
+        # Encrypt the payload with PkEncryption.
+        pke = PkEncryption(self.crypto_handler.public_key)
+        encrypted = pke.encrypt(json.dumps(payload))
+
+        # Decrypt the payload with the crypto handler.
+        decrypted = self.crypto_handler.decrypt_body(
+            encrypted.ciphertext,
+            encrypted.mac,
+            encrypted.ephemeral_key,
+        )
+
+        # Check that the decrypted payload is the same as the original one before
+        # encryption.
+        self.assertEqual(decrypted, payload)