diff --git a/plugin/src/main/java/org/elasticsearch/xpack/ml/job/process/autodetect/AutodetectProcessManager.java b/plugin/src/main/java/org/elasticsearch/xpack/ml/job/process/autodetect/AutodetectProcessManager.java
index 8b1169cb733..74a6282885e 100644
--- a/plugin/src/main/java/org/elasticsearch/xpack/ml/job/process/autodetect/AutodetectProcessManager.java
+++ b/plugin/src/main/java/org/elasticsearch/xpack/ml/job/process/autodetect/AutodetectProcessManager.java
@@ -17,6 +17,7 @@ import org.elasticsearch.common.settings.Settings;
 import org.elasticsearch.common.util.concurrent.AbstractRunnable;
 import org.elasticsearch.common.util.concurrent.EsRejectedExecutionException;
 import org.elasticsearch.common.util.concurrent.ThreadContext;
+import org.elasticsearch.common.util.set.Sets;
 import org.elasticsearch.common.xcontent.NamedXContentRegistry;
 import org.elasticsearch.common.xcontent.XContentBuilder;
 import org.elasticsearch.common.xcontent.XContentType;
@@ -299,7 +300,12 @@ public class AutodetectProcessManager extends AbstractComponent {
     }
 
     AutodetectCommunicator create(JobTask jobTask, AutodetectParams autodetectParams, Consumer<Exception> handler) {
-        if (autoDetectCommunicatorByOpenJob.size() == maxAllowedRunningJobs) {
+        // Closing jobs can still be using some or all threads in MachineLearning.AUTODETECT_THREAD_POOL_NAME
+        // that an open job uses, so include them too when considering if enough threads are available.
+        // There's a slight possibility that the same key is in both sets, hence it's not sufficient to simply
+        // add the two map sizes.
+        int currentRunningJobs = Sets.union(autoDetectCommunicatorByOpenJob.keySet(), autoDetectCommunicatorByClosingJob.keySet()).size();
+        if (currentRunningJobs >= maxAllowedRunningJobs) {
             throw new ElasticsearchStatusException("max running job capacity [" + maxAllowedRunningJobs + "] reached",
                     RestStatus.TOO_MANY_REQUESTS);
         }
@@ -379,9 +385,9 @@ public class AutodetectProcessManager extends AbstractComponent {
     }
 
     /**
-     * Stop the running job and mark it as finished.<br>
+     * Stop the running job and mark it as finished.
      *
-     * @param jobTask   The job to stop
+     * @param jobTask The job to stop
      * @param restart Whether the job should be restarted by persistent tasks
      * @param reason  The reason for closing the job
      */