diff --git a/core/insertion_marker_manager.ts b/core/insertion_marker_manager.ts
index 7438e1cb0ff..20e27d42650 100644
--- a/core/insertion_marker_manager.ts
+++ b/core/insertion_marker_manager.ts
@@ -133,6 +133,11 @@ export class InsertionMarkerManager {
     this.firstMarker = this.createMarkerBlock(this.topBlock);
 
     this.availableConnections = this.initAvailableConnections();
+
+    if (this.lastOnStack) {
+      this.lastMarker =
+          this.createMarkerBlock(this.lastOnStack.getSourceBlock());
+    }
   }
 
   /**
@@ -142,18 +147,8 @@ export class InsertionMarkerManager {
    */
   dispose() {
     this.availableConnections.length = 0;
-
-    eventUtils.disable();
-    try {
-      if (this.firstMarker) {
-        this.firstMarker.dispose();
-      }
-      if (this.lastMarker) {
-        this.lastMarker.dispose();
-      }
-    } finally {
-      eventUtils.enable();
-    }
+    this.disposeInsertionMarker(this.firstMarker);
+    this.disposeInsertionMarker(this.lastMarker);
   }
 
   /**
@@ -289,10 +284,8 @@ export class InsertionMarkerManager {
   }
 
   /**
-   * Populate the list of available connections on this block stack.  This
-   * should only be called once, at the beginning of a drag. If the stack has
-   * more than one block, this function will populate lastOnStack and create
-   * the corresponding insertion marker.
+   * Populate the list of available connections on this block stack. If the
+   * stack has more than one block, this function will also update lastOnStack.
    *
    * @returns A list of available connections.
    */
@@ -303,15 +296,6 @@ export class InsertionMarkerManager {
     if (lastOnStack && lastOnStack !== this.topBlock.nextConnection) {
       available.push(lastOnStack);
       this.lastOnStack = lastOnStack;
-      if (this.lastMarker) {
-        eventUtils.disable();
-        try {
-          this.lastMarker.dispose();
-        } finally {
-          eventUtils.enable();
-        }
-      }
-      this.lastMarker = this.createMarkerBlock(lastOnStack.getSourceBlock());
     }
     return available;
   }
@@ -561,8 +545,17 @@ export class InsertionMarkerManager {
       // probably recreate the marker block (e.g. in getCandidate_), which is
       // called more often during the drag, but creating a block that often
       // might be too slow, so we only do it if necessary.
-      this.firstMarker = this.createMarkerBlock(this.topBlock);
-      insertionMarker = isLastInStack ? this.lastMarker : this.firstMarker;
+      if (isLastInStack && this.lastOnStack) {
+        this.disposeInsertionMarker(this.lastMarker);
+        this.lastMarker =
+            this.createMarkerBlock(this.lastOnStack.getSourceBlock());
+        insertionMarker = this.lastMarker;
+      } else {
+        this.disposeInsertionMarker(this.firstMarker);
+        this.firstMarker = this.createMarkerBlock(this.topBlock);
+        insertionMarker = this.firstMarker;
+      }
+
       if (!insertionMarker) {
         throw new Error(
             'Cannot show the insertion marker because there is no insertion ' +
@@ -728,6 +721,20 @@ export class InsertionMarkerManager {
     }
     return result;
   }
+
+  /**
+   * Safely disposes of an insertion marker.
+   */
+  private disposeInsertionMarker(marker: BlockSvg|null) {
+    if (marker) {
+      eventUtils.disable();
+      try {
+        marker.dispose();
+      } finally {
+        eventUtils.enable();
+      }
+    }
+  }
 }
 
 export namespace InsertionMarkerManager {