diff --git a/.changeset/swift-lobsters-mate.md b/.changeset/swift-lobsters-mate.md
new file mode 100644
index 00000000000..752fa93ad48
--- /dev/null
+++ b/.changeset/swift-lobsters-mate.md
@@ -0,0 +1,5 @@
+---
+'@keystonejs/keystone': patch
+---
+
+Added a check for invalid relationship configurations.
diff --git a/.changeset/unlucky-swans-deliver.md b/.changeset/unlucky-swans-deliver.md
new file mode 100644
index 00000000000..c1286c9e6d3
--- /dev/null
+++ b/.changeset/unlucky-swans-deliver.md
@@ -0,0 +1,5 @@
+---
+'@keystonejs/fields': patch
+---
+
+Updated internal relationship configurations of `Content` fields to be self-consistent.
diff --git a/packages/fields/src/types/CloudinaryImage/ImageBlock.js b/packages/fields/src/types/CloudinaryImage/ImageBlock.js
index 7043548c177..073e621ff1c 100644
--- a/packages/fields/src/types/CloudinaryImage/ImageBlock.js
+++ b/packages/fields/src/types/CloudinaryImage/ImageBlock.js
@@ -83,7 +83,7 @@ export class ImageBlock extends Block {
     return {
       [this.path]: {
         type: RelationshipWrapper,
-        ref: this.auxList.key,
+        ref: `${this.auxList.key}.from`,
         many: true,
         schemaDoc: 'Images which have been added to the Content field',
       },
diff --git a/packages/fields/src/types/OEmbed/OEmbedBlock.js b/packages/fields/src/types/OEmbed/OEmbedBlock.js
index d1c9172f087..3459982a7aa 100644
--- a/packages/fields/src/types/OEmbed/OEmbedBlock.js
+++ b/packages/fields/src/types/OEmbed/OEmbedBlock.js
@@ -69,7 +69,7 @@ export class OEmbedBlock extends Block {
     return {
       [this.path]: {
         type: RelationshipWrapper,
-        ref: this.auxList.key,
+        ref: `${this.auxList.key}.from`,
         many: true,
         schemaDoc: 'Embeds which have been added to the Content field',
       },
diff --git a/packages/fields/src/types/Unsplash/UnsplashBlock.js b/packages/fields/src/types/Unsplash/UnsplashBlock.js
index ce453518e2a..6bd7803c614 100644
--- a/packages/fields/src/types/Unsplash/UnsplashBlock.js
+++ b/packages/fields/src/types/Unsplash/UnsplashBlock.js
@@ -81,7 +81,7 @@ export class UnsplashBlock extends Block {
     return {
       [this.path]: {
         type: RelationshipWrapper,
-        ref: this.auxList.key,
+        ref: `${this.auxList.key}.from`,
         many: true,
         schemaDoc: 'Unsplash Images which have been added to the Content field',
       },
diff --git a/packages/keystone/lib/Keystone/index.js b/packages/keystone/lib/Keystone/index.js
index 63f221ddb4a..0543943cdd2 100644
--- a/packages/keystone/lib/Keystone/index.js
+++ b/packages/keystone/lib/Keystone/index.js
@@ -313,6 +313,45 @@ module.exports = class Keystone {
     this._extendedMutations = this._extendedMutations.concat(mutations.map(_parseAccess));
   }
 
+  _consolidateRelationships() {
+    const rels = {};
+    const otherSides = {};
+    this.listsArray.forEach(list => {
+      list.fields
+        .filter(f => f.isRelationship)
+        .forEach(f => {
+          const myRef = `${f.listKey}.${f.path}`;
+          if (otherSides[myRef]) {
+            // I'm already there, go and update rels[otherSides[myRef]] with my info
+            rels[otherSides[myRef]].right = f;
+
+            // Make sure I'm actually referencing the thing on the left
+            const { left } = rels[otherSides[myRef]];
+            if (f.config.ref !== `${left.listKey}.${left.path}`) {
+              throw new Error(
+                `${myRef} refers to ${f.config.ref}. Expected ${left.listKey}.${left.path}`
+              );
+            }
+          } else {
+            // Got us a new relationship!
+            rels[myRef] = { left: f };
+            if (f.refFieldPath) {
+              // Populate otherSides
+              otherSides[f.config.ref] = myRef;
+            }
+          }
+        });
+    });
+    // See if anything failed to link up.
+    const badRel = Object.values(rels).find(({ left, right }) => left.refFieldPath && !right);
+    if (badRel) {
+      const { left } = badRel;
+      throw new Error(
+        `${left.listKey}.${left.path} refers to a non-existant field, ${left.config.ref}`
+      );
+    }
+  }
+
   /**
    * @return Promise<null>
    */
@@ -684,6 +723,7 @@ module.exports = class Keystone {
     pinoOptions,
     cors = { origin: true, credentials: true },
   } = {}) {
+    this._consolidateRelationships();
     const middlewares = flattenDeep([
       this.appVersion.addVersionToHttpHeaders &&
         ((req, res, next) => {